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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Effect of Metals, Metalloids and Metallic Nanoparticles on Microalgae Growth and Industrial Product Biosynthesis: A Review</title><author><name sortKey="Miazek, Krystian" sort="Miazek, Krystian" uniqKey="Miazek K" first="Krystian" last="Miazek">Krystian Miazek</name><affiliation><nlm:aff id="af1-ijms-16-23929">AgricultureIsLife Platform, University of Liege-Gembloux Agro-Bio Tech, Passage des Déportés 2, Gembloux B-5030, Belgium</nlm:aff></affiliation></author><author><name sortKey="Iwanek, Waldemar" sort="Iwanek, Waldemar" uniqKey="Iwanek W" first="Waldemar" last="Iwanek">Waldemar Iwanek</name><affiliation><nlm:aff id="af2-ijms-16-23929">Faculty of Mathematics and Natural Sciences, the Jan Kochanowski University in Kielce, Swietokrzyska 15, Kielce 25-406, Poland; E-Mail:<email>iwanek@pu.kielce.pl</email></nlm:aff></affiliation></author><author><name sortKey="Remacle, Claire" sort="Remacle, Claire" uniqKey="Remacle C" first="Claire" last="Remacle">Claire Remacle</name><affiliation><nlm:aff id="af3-ijms-16-23929">Genetics and Physiology of Microalgae, Institute of Botany, University of Liege, B22, 27, Bld du Rectorat, Liège B-4000, Belgium; E-Mail:<email>c.remacle@ulg.ac.be</email></nlm:aff></affiliation></author><author><name sortKey="Richel, Aurore" sort="Richel, Aurore" uniqKey="Richel A" first="Aurore" last="Richel">Aurore Richel</name><affiliation><nlm:aff id="af4-ijms-16-23929">Unit of Biological and Industrial Chemistry, University of Liege-Gembloux Agro-Bio Tech, Passage des Déportés 2, Gembloux B-5030, Belgium; E-Mail:<email>a.richel@ulg.ac.be</email></nlm:aff></affiliation></author><author><name sortKey="Goffin, Dorothee" sort="Goffin, Dorothee" uniqKey="Goffin D" first="Dorothee" last="Goffin">Dorothee Goffin</name><affiliation><nlm:aff id="af5-ijms-16-23929">Cellule Innovation et Créativité, University of Liege-Gembloux Agro-Bio Tech, Passage des Déportés 2, Gembloux B-5030, Belgium; E-Mail:<email>dorothee.goffin@ulg.ac.be</email></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26473834</idno><idno type="pmc">4632732</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4632732</idno><idno type="RBID">PMC:4632732</idno><idno type="doi">10.3390/ijms161023929</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000048</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000048</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Effect of Metals, Metalloids and Metallic Nanoparticles on Microalgae Growth and Industrial Product Biosynthesis: A Review</title><author><name sortKey="Miazek, Krystian" sort="Miazek, Krystian" uniqKey="Miazek K" first="Krystian" last="Miazek">Krystian Miazek</name><affiliation><nlm:aff id="af1-ijms-16-23929">AgricultureIsLife Platform, University of Liege-Gembloux Agro-Bio Tech, Passage des Déportés 2, Gembloux B-5030, Belgium</nlm:aff></affiliation></author><author><name sortKey="Iwanek, Waldemar" sort="Iwanek, Waldemar" uniqKey="Iwanek W" first="Waldemar" last="Iwanek">Waldemar Iwanek</name><affiliation><nlm:aff id="af2-ijms-16-23929">Faculty of Mathematics and Natural Sciences, the Jan Kochanowski University in Kielce, Swietokrzyska 15, Kielce 25-406, Poland; E-Mail:<email>iwanek@pu.kielce.pl</email></nlm:aff></affiliation></author><author><name sortKey="Remacle, Claire" sort="Remacle, Claire" uniqKey="Remacle C" first="Claire" last="Remacle">Claire Remacle</name><affiliation><nlm:aff id="af3-ijms-16-23929">Genetics and Physiology of Microalgae, Institute of Botany, University of Liege, B22, 27, Bld du Rectorat, Liège B-4000, Belgium; E-Mail:<email>c.remacle@ulg.ac.be</email></nlm:aff></affiliation></author><author><name sortKey="Richel, Aurore" sort="Richel, Aurore" uniqKey="Richel A" first="Aurore" last="Richel">Aurore Richel</name><affiliation><nlm:aff id="af4-ijms-16-23929">Unit of Biological and Industrial Chemistry, University of Liege-Gembloux Agro-Bio Tech, Passage des Déportés 2, Gembloux B-5030, Belgium; E-Mail:<email>a.richel@ulg.ac.be</email></nlm:aff></affiliation></author><author><name sortKey="Goffin, Dorothee" sort="Goffin, Dorothee" uniqKey="Goffin D" first="Dorothee" last="Goffin">Dorothee Goffin</name><affiliation><nlm:aff id="af5-ijms-16-23929">Cellule Innovation et Créativité, University of Liege-Gembloux Agro-Bio Tech, Passage des Déportés 2, Gembloux B-5030, Belgium; E-Mail:<email>dorothee.goffin@ulg.ac.be</email></nlm:aff></affiliation></author></analytic><series><title level="j">International Journal of Molecular Sciences</title><idno type="eISSN">1422-0067</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Microalgae are a source of numerous compounds that can be used in many branches of industry. Synthesis of such compounds in microalgal cells can be amplified under stress conditions. Exposure to various metals can be one of methods applied to induce cell stress and synthesis of target products in microalgae cultures. In this review, the potential of producing diverse biocompounds (pigments, lipids, exopolymers, peptides, phytohormones, arsenoorganics, nanoparticles) from microalgae cultures upon exposure to various metals, is evaluated. Additionally, different methods to alter microalgae response towards metals and metal stress are described. Finally, possibilities to sustain high growth rates and productivity of microalgal cultures in the presence of metals are discussed.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Leliaert, F" uniqKey="Leliaert F">F. Leliaert</name></author><author><name sortKey="Smith, D R" uniqKey="Smith D">D.R. Smith</name></author><author><name sortKey="Moreau, H" uniqKey="Moreau H">H. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Int J Mol Sci</journal-id><journal-id journal-id-type="iso-abbrev">Int J Mol Sci</journal-id><journal-id journal-id-type="publisher-id">ijms</journal-id><journal-title-group><journal-title>International Journal of Molecular Sciences</journal-title></journal-title-group><issn pub-type="epub">1422-0067</issn><publisher><publisher-name>MDPI</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26473834</article-id><article-id pub-id-type="pmc">4632732</article-id><article-id pub-id-type="doi">10.3390/ijms161023929</article-id><article-id pub-id-type="publisher-id">ijms-16-23929</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>Effect of Metals, Metalloids and Metallic Nanoparticles on Microalgae Growth and Industrial Product Biosynthesis: A Review</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Miazek</surname><given-names>Krystian</given-names></name><xref ref-type="aff" rid="af1-ijms-16-23929">1</xref><xref rid="c1-ijms-16-23929" ref-type="corresp">*</xref></contrib><contrib contrib-type="author"><name><surname>Iwanek</surname><given-names>Waldemar</given-names></name><xref ref-type="aff" rid="af2-ijms-16-23929">2</xref></contrib><contrib contrib-type="author"><name><surname>Remacle</surname><given-names>Claire</given-names></name><xref ref-type="aff" rid="af3-ijms-16-23929">3</xref></contrib><contrib contrib-type="author"><name><surname>Richel</surname><given-names>Aurore</given-names></name><xref ref-type="aff" rid="af4-ijms-16-23929">4</xref></contrib><contrib contrib-type="author"><name><surname>Goffin</surname><given-names>Dorothee</given-names></name><xref ref-type="aff" rid="af5-ijms-16-23929">5</xref></contrib></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>Lan</surname><given-names>Christopher Q.</given-names></name><role>Academic Editor</role></contrib></contrib-group><aff id="af1-ijms-16-23929"><label>1</label>AgricultureIsLife Platform, University of Liege-Gembloux Agro-Bio Tech, Passage des Déportés 2, Gembloux B-5030, Belgium</aff><aff id="af2-ijms-16-23929"><label>2</label>Faculty of Mathematics and Natural Sciences, the Jan Kochanowski University in Kielce, Swietokrzyska 15, Kielce 25-406, Poland; E-Mail:<email>iwanek@pu.kielce.pl</email></aff><aff id="af3-ijms-16-23929"><label>3</label>Genetics and Physiology of Microalgae, Institute of Botany, University of Liege, B22, 27, Bld du Rectorat, Liège B-4000, Belgium; E-Mail:<email>c.remacle@ulg.ac.be</email></aff><aff id="af4-ijms-16-23929"><label>4</label>Unit of Biological and Industrial Chemistry, University of Liege-Gembloux Agro-Bio Tech, Passage des Déportés 2, Gembloux B-5030, Belgium; E-Mail:<email>a.richel@ulg.ac.be</email></aff><aff id="af5-ijms-16-23929"><label>5</label>Cellule Innovation et Créativité, University of Liege-Gembloux Agro-Bio Tech, Passage des Déportés 2, Gembloux B-5030, Belgium; E-Mail:<email>dorothee.goffin@ulg.ac.be</email></aff><author-notes><corresp id="c1-ijms-16-23929"><label>*</label>Author to whom correspondence should be addressed; E-Mail: <email>kmiazek@ulg.ac.be</email>; Tel.: +48-60-817-8511.</corresp></author-notes><pub-date pub-type="epub"><day>09</day><month>10</month><year>2015</year></pub-date><pub-date pub-type="collection"><month>10</month><year>2015</year></pub-date><volume>16</volume><issue>10</issue><fpage>23929</fpage><lpage>23969</lpage><history><date date-type="received"><day>18</day><month>8</month><year>2015</year></date><date date-type="accepted"><day>24</day><month>9</month><year>2015</year></date></history><permissions><copyright-statement>© 2015 by the authors; licensee MDPI, Basel, Switzerland.</copyright-statement><copyright-year>2015</copyright-year><license><license-p><pmc-comment>CREATIVE COMMONS</pmc-comment>This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>).</license-p></license></permissions><abstract><p>Microalgae are a source of numerous compounds that can be used in many branches of industry. Synthesis of such compounds in microalgal cells can be amplified under stress conditions. Exposure to various metals can be one of methods applied to induce cell stress and synthesis of target products in microalgae cultures. In this review, the potential of producing diverse biocompounds (pigments, lipids, exopolymers, peptides, phytohormones, arsenoorganics, nanoparticles) from microalgae cultures upon exposure to various metals, is evaluated. Additionally, different methods to alter microalgae response towards metals and metal stress are described. Finally, possibilities to sustain high growth rates and productivity of microalgal cultures in the presence of metals are discussed.</p></abstract><kwd-group><kwd>microalgae</kwd><kwd>metal stress</kwd><kwd>industrial products</kwd><kwd>growth rate</kwd><kwd>metal resistance</kwd></kwd-group></article-meta></front><body><sec id="sec1-ijms-16-23929"><title>1. Introduction</title><p>Microalgae are photosynthetic microorganisms, using solar light to convert CO<sub>2</sub> from the atmosphere into organic carbon. There are eukaryotic microalgae such as green microalgae [<xref rid="B1-ijms-16-23929" ref-type="bibr">1</xref>], red microalgae [<xref rid="B2-ijms-16-23929" ref-type="bibr">2</xref>], diatoms [<xref rid="B3-ijms-16-23929" ref-type="bibr">3</xref>] and dinoflagellates [<xref rid="B4-ijms-16-23929" ref-type="bibr">4</xref>] or prokaryotic cyanobacteria [<xref rid="B5-ijms-16-23929" ref-type="bibr">5</xref>]. Some of them are capable of growing mixotrophically or heterotrophically because they use sugars, glycerol or organic acids as their carbon source [<xref rid="B6-ijms-16-23929" ref-type="bibr">6</xref>]. The optimal temperature for microalgae growth is usually 20–30 °C, but it is also reported that some strains are able to grow at much lower [<xref rid="B7-ijms-16-23929" ref-type="bibr">7</xref>] or higher [<xref rid="B8-ijms-16-23929" ref-type="bibr">8</xref>] temperature conditions. Microalgae are a source of valuable compounds such as lipids, pigments, carbohydrates, vitamins, and proteins, with potential applications in many branches of industry. Nowadays, research is focused on improving synthesis and maximizing production of valuable compounds from microalgae cultures. Microalgal cells are able to synthetize numerous compounds in higher amounts, as a response to stress conditions such as high temperature, high salinity, nutrient starvation, and also metal stress. However, stress conditions can also have negative effects on microalgae growth [<xref rid="B9-ijms-16-23929" ref-type="bibr">9</xref>,<xref rid="B10-ijms-16-23929" ref-type="bibr">10</xref>].</p><p>Human activity, development of industry and natural Earth processess lead to release of numerous metals (Fe, Zn, Cu, Cd, Cr, Ni, Hg, Pb, La, Li, V), metalloids (As, Te) and metallic nanoparticles (Ag, Pt, TiO<sub>2</sub>, ZnO, CeO<sub>2</sub>, NiO, BaTiO<sub>3</sub>, Y<sub>2</sub>O<sub>3</sub>, Al<sub>2</sub>O<sub>3</sub>) [<xref rid="B11-ijms-16-23929" ref-type="bibr">11</xref>,<xref rid="B12-ijms-16-23929" ref-type="bibr">12</xref>,<xref rid="B13-ijms-16-23929" ref-type="bibr">13</xref>,<xref rid="B14-ijms-16-23929" ref-type="bibr">14</xref>,<xref rid="B15-ijms-16-23929" ref-type="bibr">15</xref>,<xref rid="B16-ijms-16-23929" ref-type="bibr">16</xref>] that can act as stressors or modulators for microalgae growth and metabolism. This review presents advantages and disadvantages of metal stress, as a possible method to produce industrial compounds from microalgae cultures.</p></sec><sec id="sec2-ijms-16-23929"><title>2. Effect of Metals on Microalgae: Growth Inhibition <italic>vs.</italic> Growth Enhancement</title><p>Metals at small concentrations are indispensable for microalgae cells to perform cellular functions. They act as components for photosynthetic electron transport proteins (Cu, Fe) and photosynthetic water oxidizing centres (Mn) or are constituents of vitamins (Co) [<xref rid="B17-ijms-16-23929" ref-type="bibr">17</xref>]. They also serve as cofactors for enzymes participating in CO<sub>2</sub> fixation (Zn in carbonic anhydrase) [<xref rid="B18-ijms-16-23929" ref-type="bibr">18</xref>], DNA transcription (Zn in RNA polymerase) and phosphorus acquisition (Zn in alkaline phosphatase) [<xref rid="B19-ijms-16-23929" ref-type="bibr">19</xref>] or N<sub>2</sub> assimilation (Mo, Fe, V in nitrogenase) [<xref rid="B20-ijms-16-23929" ref-type="bibr">20</xref>] and nitrate reduction (Mo in nitrate and Fe in nitrite reductase) [<xref rid="B21-ijms-16-23929" ref-type="bibr">21</xref>]. However, high concentrations of these metals, and other non-essential heavy metals (Hg, As, Cd, Pb, Cr) cause negative effects (impairment of photosynthetic mechanism, blockage of cell division, inhibition of enzyme activity) in microalgae cells [<xref rid="B12-ijms-16-23929" ref-type="bibr">12</xref>]. Metals also influence the morphology of microalgal cells. Accumulation of cadmium (Cd) in <italic>Chlamydomonas acidophila</italic> cells resulted in the increase in cell size and decomposition of polyphosphate bodies [<xref rid="B22-ijms-16-23929" ref-type="bibr">22</xref>]. The presence of lead (Pb) in <italic>Chlorella sorokiniana</italic> culture resulted in the formation of colonies of <italic>Chlorella</italic> cells possessing cytoplasm lipid droplets and misshaped chloroplasts [<xref rid="B23-ijms-16-23929" ref-type="bibr">23</xref>]. Fragmentation of thylakoid membranes was observed in <italic>Synechocystis</italic> sp. cells upon exposure to thallium (Tl) [<xref rid="B24-ijms-16-23929" ref-type="bibr">24</xref>]. Mitochondria in <italic>Desmidium swartzii</italic> cells became enlarged and bloated, upon cell exposure to Zn [<xref rid="B25-ijms-16-23929" ref-type="bibr">25</xref>]. Synergistic effect of aluminum (Al) and lead on <italic>Dunaliella tertiolecta</italic> caused cell membrane lysis [<xref rid="B26-ijms-16-23929" ref-type="bibr">26</xref>]. Cerium (Ce)-associated cell damage in <italic>Anabaena flosaquae</italic>, can additionally lead to the release of toxins [<xref rid="B27-ijms-16-23929" ref-type="bibr">27</xref>]. Lithium (Li) can alter the length and form of flagella in <italic>Chlamydomonas reinhardtii</italic> [<xref rid="B28-ijms-16-23929" ref-type="bibr">28</xref>] or affect the structure of polysaccharide sheath around <italic>Ankistrodesmus gracilis</italic> cells [<xref rid="B29-ijms-16-23929" ref-type="bibr">29</xref>], and can also at various concentrations inhibit other microalgae strains [<xref rid="B30-ijms-16-23929" ref-type="bibr">30</xref>,<xref rid="B31-ijms-16-23929" ref-type="bibr">31</xref>]. Cultivation of diatom <italic>Synedra acus</italic> in the presence of germanium (Ge), titanium (Ti), zirconium (Zr) or tin (Sn) caused alterations in shape, size and mechanical strength of silica valves in <italic>Synedra</italic> frustules [<xref rid="B32-ijms-16-23929" ref-type="bibr">32</xref>].</p><p>Although heavy metals generally have negative effect on microalgae cultures, some reports suggest also their positive role during microalgae cultivation (<xref ref-type="table" rid="ijms-16-23929-t001">Table 1</xref>). Lead, aluminum [<xref rid="B26-ijms-16-23929" ref-type="bibr">26</xref>] and cobalt [<xref rid="B33-ijms-16-23929" ref-type="bibr">33</xref>] at low concentrations had stimulatory effect on growth of <italic>Dunaliella tertiolecta</italic> [<xref rid="B26-ijms-16-23929" ref-type="bibr">26</xref>] and <italic>Monoraphidium</italic><italic>minutum</italic> [<xref rid="B33-ijms-16-23929" ref-type="bibr">33</xref>]. Arsenic (As(V)) was reported to improve the growth of cyanobacterium <italic>Nostoc minutum</italic> [<xref rid="B34-ijms-16-23929" ref-type="bibr">34</xref>] and microalgae <italic>Chlorella salina</italic> [<xref rid="B35-ijms-16-23929" ref-type="bibr">35</xref>] and <italic>Chlorella</italic> sp. [<xref rid="B36-ijms-16-23929" ref-type="bibr">36</xref>]. What is more, inorganics can support microalgae growth in case of nutrient deficiency. For instance, 20 µg/L vanadium (VO<sub>3</sub><sup>−</sup>) increased growth of <italic>Scenedesmus obliquus</italic> grown in iron (Fe<sup>3+</sup>) deficient medium up to six times. Vanadium was almost entirely consumed by <italic>Scenedesmus</italic> cells under photoautotrophic cultivation conditions [<xref rid="B37-ijms-16-23929" ref-type="bibr">37</xref>]. In another study, addition of 0.01–1 µg/L vanadium (VO<sub>3</sub><sup>−</sup>) resulted in up to 67% growth enhancement in photoautotrophic <italic>Chlorella pyrenoidosa</italic> culture, even with iron (Fe<sup>3+</sup>) supplementation in the growth media [<xref rid="B38-ijms-16-23929" ref-type="bibr">38</xref>]. However, vanadium (VO<sub>3</sub><sup>−</sup>) at concentrations above 1 mg/L was inhibitory for <italic>Chlorella pyrenoidosa</italic> [<xref rid="B38-ijms-16-23929" ref-type="bibr">38</xref>]. Vanadium, in a form of VO<sub>4</sub><sup>3−</sup> [<xref rid="B39-ijms-16-23929" ref-type="bibr">39</xref>] and V<sub>2</sub>O<sub>5</sub> [<xref rid="B40-ijms-16-23929" ref-type="bibr">40</xref>], was also reported to be inhibitory to <italic>Haematococcus lacustris</italic> [<xref rid="B39-ijms-16-23929" ref-type="bibr">39</xref>] and <italic>Scenedesmus quadricauda</italic> [<xref rid="B40-ijms-16-23929" ref-type="bibr">40</xref>].</p><p>Furthermore, elements from the lanthanide group such as lanthanum (La), cerium (Ce), neodynium (Nd), europium (Eu) or gadolinium (Gd) were reported to constitute a good replacement for calcium deficiency in <italic>Desmodesmus quadricauda</italic> culture, with Gd, La or Nd supplementation leading to nearly the same culture dry weight when compared to Ca supplemented media. Moreover, addition of cerium at low concentration to standard medium increased <italic>Desmodesmus</italic> cell number in culture. However, lanthanide elements increased growth suppression of <italic>Desmodesmus</italic>, when added into manganese deficient medium [<xref rid="B41-ijms-16-23929" ref-type="bibr">41</xref>]. Also lanthanum at higher concentration inhibited growth of <italic>Scenedesmus quadricauda</italic> [<xref rid="B42-ijms-16-23929" ref-type="bibr">42</xref>] or <italic>Sceletonema costatum</italic> [<xref rid="B43-ijms-16-23929" ref-type="bibr">43</xref>], and inhibitory concentration of La was the same as for other lanthanides: cerium (Ce), neodymium (Nd), samarium (Sm), europium (Eu), gadolinium (Gd), terbium (Tb), dysprosium (Dy), holmium (Ho), erbium (Er), thulium (Tm), ytterbium (Yb) and lutetium (Lu) [<xref rid="B43-ijms-16-23929" ref-type="bibr">43</xref>]. Cerium (Ce) was stimulatory at lower concentration and inhibitory at higher concentration towards cyanobacterium <italic>Anabaena flosaquae</italic> [<xref rid="B27-ijms-16-23929" ref-type="bibr">27</xref>].</p><p>Cd<sup>2+</sup> at small concentrations was reported to stimulate growth and maintain activity of carbonic anhydrase in <italic>Thalassiosira weissflogii</italic> cells, cultivated in Zn-limited medium [<xref rid="B44-ijms-16-23929" ref-type="bibr">44</xref>]. Recently, a novel carbonic anhydrase naturally possesing Cd<sup>2+</sup> as a catalytic metal ion, has been discovered in <italic>Thalassiosira weissflogii</italic> [<xref rid="B45-ijms-16-23929" ref-type="bibr">45</xref>].</p><p>Ni<sup>2+</sup> is an essential metal for cultivation of marine diatoms such as <italic>Phaeodactylum tricornutum</italic> [<xref rid="B46-ijms-16-23929" ref-type="bibr">46</xref>], <italic>Cyclotella cryptica</italic> [<xref rid="B47-ijms-16-23929" ref-type="bibr">47</xref>], <italic>Thalassiosira weissflogii</italic> and <italic>Thalassiosira pseudonana</italic> [<xref rid="B48-ijms-16-23929" ref-type="bibr">48</xref>], in the presence of urea as a sole nitrogen source. Nickel serves as a cofactor in an enzyme urease, but Ni at higher concentations was inhibitory for diatom growth [<xref rid="B47-ijms-16-23929" ref-type="bibr">47</xref>,<xref rid="B48-ijms-16-23929" ref-type="bibr">48</xref>]. A lack of Ni can be partially substituted by cobalt [<xref rid="B46-ijms-16-23929" ref-type="bibr">46</xref>].</p><p>In addition to metals and metalloids, also metallic nanoparticles (NPs) exert activity towards microalgae. Inhibitory effects of TiO<sub>2</sub>, ZnO, CeO<sub>2</sub>, NiO, BaTiO<sub>3</sub>, Y<sub>2</sub>O<sub>3</sub>, Al<sub>2</sub>O<sub>3</sub>, Ag and Pt nanoparticles were reported towards numerous freshwater and marine microalgae strains and their inhibitory activity was suggested to be due to Reactive Oxygen Species (ROS) generation [<xref rid="B49-ijms-16-23929" ref-type="bibr">49</xref>,<xref rid="B50-ijms-16-23929" ref-type="bibr">50</xref>] or mechanical damage caused by nanoparticles themselves [<xref rid="B51-ijms-16-23929" ref-type="bibr">51</xref>], but also due to metal ions released from nanoparticles [<xref rid="B50-ijms-16-23929" ref-type="bibr">50</xref>,<xref rid="B52-ijms-16-23929" ref-type="bibr">52</xref>,<xref rid="B53-ijms-16-23929" ref-type="bibr">53</xref>], light shading effect [<xref rid="B54-ijms-16-23929" ref-type="bibr">54</xref>], interactions with growth media components [<xref rid="B55-ijms-16-23929" ref-type="bibr">55</xref>] or simultaneous effect of various factors [<xref rid="B56-ijms-16-23929" ref-type="bibr">56</xref>]. Inhibitory activity of nanoparticles also depends on their size [<xref rid="B49-ijms-16-23929" ref-type="bibr">49</xref>] and aged suspension [<xref rid="B55-ijms-16-23929" ref-type="bibr">55</xref>] or growth medium composition [<xref rid="B53-ijms-16-23929" ref-type="bibr">53</xref>]. On the other hand, metal ions released from nanoparticles can also stimulate growth of cyanobacteria and microalgae [<xref rid="B57-ijms-16-23929" ref-type="bibr">57</xref>].</p><table-wrap id="ijms-16-23929-t001" position="float"><object-id pub-id-type="pii">ijms-16-23929-t001_Table 1</object-id><label>Table 1</label><caption><p>Effect of metals, metalloids and metallic nanoparticles on growth of microalgae.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Metal</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Microalgae Strain</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Cultivation Time</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Concentration</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Effect on Growth</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Ref.</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Hg</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella</italic> sp. <italic>Scenedesmus acutus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">8 days</td><td align="center" valign="middle" rowspan="1" colspan="1">2.5–5 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">100% growth inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B58-ijms-16-23929" ref-type="bibr">58</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Hg</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Selenastrum capricornutum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">–</td><td align="center" valign="middle" rowspan="1" colspan="1">0.027 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B59-ijms-16-23929" ref-type="bibr">59</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Pb</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Phaeocystis antarctica</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">10 days</td><td align="center" valign="middle" rowspan="1" colspan="1">0.57 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B60-ijms-16-23929" ref-type="bibr">60</xref>]</td></tr><tr><td rowspan="2" align="center" valign="middle" colspan="1">Pb</td><td rowspan="2" align="center" valign="middle" colspan="1"><italic>Dunaliella tertiolecta</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">48 h</td><td align="center" valign="middle" rowspan="1" colspan="1">1.5–6.4 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">20% stimulation</td><td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B26-ijms-16-23929" ref-type="bibr">26</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">48 h</td><td align="center" valign="middle" rowspan="1" colspan="1">7.29 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">25% inhibition</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Cr(III)</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Dyctiosphaerium chlorelloides</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">13–17 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B61-ijms-16-23929" ref-type="bibr">61</xref>]</td></tr><tr><td rowspan="2" align="center" valign="middle" colspan="1">Cr(III)</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Scenedesmus</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">9 days</td><td align="center" valign="middle" rowspan="1" colspan="1">0.75 µM</td><td rowspan="2" align="center" valign="middle" colspan="1">MMC</td><td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B62-ijms-16-23929" ref-type="bibr">62</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Geitlerinema</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">9 days</td><td align="center" valign="middle" rowspan="1" colspan="1">0.25 µM</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Cr(VI)</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella pyrenoidosa</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">2 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B63-ijms-16-23929" ref-type="bibr">63</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Cr(VI)</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">96 h</td><td align="center" valign="middle" rowspan="1" colspan="1">5 µmol/L</td><td align="center" valign="middle" rowspan="1" colspan="1">~40% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B64-ijms-16-23929" ref-type="bibr">64</xref>]</td></tr><tr><td rowspan="2" align="center" valign="middle" colspan="1">As(III)</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">25.2 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B65-ijms-16-23929" ref-type="bibr">65</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Monoraphidium arcuatum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">14.6 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">As(III)</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">27 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B66-ijms-16-23929" ref-type="bibr">66</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">As(V)</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">1.1 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B66-ijms-16-23929" ref-type="bibr">66</xref>]</td></tr><tr><td rowspan="2" align="center" valign="middle" colspan="1">As(V)</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">25.4 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B65-ijms-16-23929" ref-type="bibr">65</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Monoraphidium arcuatum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">0.254 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td></tr><tr><td rowspan="3" align="center" valign="middle" colspan="1">As(V)</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Oscillatoria tenuisa</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">3.8 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td rowspan="3" align="center" valign="middle" colspan="1">[<xref rid="B67-ijms-16-23929" ref-type="bibr">67</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Anabaena affinis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">2.6 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Microcystis aeruginosa</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">1.2 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">As(III)</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Nostoc minutum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">7 days</td><td align="center" valign="middle" rowspan="1" colspan="1">5 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">Cell death</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B34-ijms-16-23929" ref-type="bibr">34</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">As(V)</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Nostoc minutum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">7 days</td><td align="center" valign="middle" rowspan="1" colspan="1">1000 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">66% stimulation</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B34-ijms-16-23929" ref-type="bibr">34</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Cu</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Isochrysis galbana</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">0.01–0.018 mg/L <sup>T</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B68-ijms-16-23929" ref-type="bibr">68</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Cu</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Phaeocystis antarctica</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">10 days</td><td align="center" valign="middle" rowspan="1" colspan="1">0.0059 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B60-ijms-16-23929" ref-type="bibr">60</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Cd</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Phaeocystis antarctica</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">10 days</td><td align="center" valign="middle" rowspan="1" colspan="1">1.5 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B60-ijms-16-23929" ref-type="bibr">60</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Cd</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Scenedesmus armatus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">24 h</td><td align="center" valign="middle" rowspan="1" colspan="1">~15–18 mg/L <sup>+</sup> or 0.46–0.54 mg/L <sup>+x</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B69-ijms-16-23929" ref-type="bibr">69</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Cd</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Thalassiosira weissflogii</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">–</td><td align="center" valign="middle" rowspan="1" colspan="1">4.6 pM</td><td align="center" valign="middle" rowspan="1" colspan="1">~30%–92% stimulation <sup>ZnL</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B44-ijms-16-23929" ref-type="bibr">44</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Ni</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Selenastrum capricornutum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">–</td><td align="center" valign="middle" rowspan="1" colspan="1">0.125 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B59-ijms-16-23929" ref-type="bibr">59</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Ni</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Synechococcus</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">15 day</td><td align="center" valign="middle" rowspan="1" colspan="1">25 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">~42% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B70-ijms-16-23929" ref-type="bibr">70</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Li</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella vannielii</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">12 h</td><td align="center" valign="middle" rowspan="1" colspan="1">1000 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">48% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B30-ijms-16-23929" ref-type="bibr">30</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Li</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Cyanothece</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">28 days</td><td align="center" valign="middle" rowspan="1" colspan="1">70 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">Cell death</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B31-ijms-16-23929" ref-type="bibr">31</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Tl</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">80 nmol</td><td align="center" valign="middle" rowspan="1" colspan="1">100% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B71-ijms-16-23929" ref-type="bibr">71</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Tl</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Synechocystis</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">1 µM</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B72-ijms-16-23929" ref-type="bibr">72</xref>]</td></tr><tr><td rowspan="2" align="center" valign="middle" colspan="1">Co</td><td rowspan="2" align="center" valign="middle" colspan="1"><italic>Monoraphidium minutum</italic></td><td rowspan="2" align="center" valign="middle" colspan="1">11 days</td><td align="center" valign="middle" rowspan="1" colspan="1">0.5 ppm</td><td align="center" valign="middle" rowspan="1" colspan="1">12% stimulation</td><td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B33-ijms-16-23929" ref-type="bibr">33</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">3 ppm</td><td align="center" valign="middle" rowspan="1" colspan="1">44% inhibition</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Zn</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Phaeocystis antarctica</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">10 days</td><td align="center" valign="middle" rowspan="1" colspan="1">1.11 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B60-ijms-16-23929" ref-type="bibr">60</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Zn</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Anabaena</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">96 h</td><td align="center" valign="middle" rowspan="1" colspan="1">0.38 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B73-ijms-16-23929" ref-type="bibr">73</xref>]</td></tr><tr><td rowspan="2" align="center" valign="middle" colspan="1">Al</td><td rowspan="2" align="center" valign="middle" colspan="1"><italic>Dunaliella tertiolecta</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">48 h</td><td align="center" valign="middle" rowspan="1" colspan="1">2.6–14.9 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">20% stimulation</td><td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B26-ijms-16-23929" ref-type="bibr">26</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">48 h</td><td align="center" valign="middle" rowspan="1" colspan="1">22.42 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">25% inhibition</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Al</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Isochrysis galbana</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">2.57–3.23 mg/L <sup>T</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B68-ijms-16-23929" ref-type="bibr">68</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">V <sup>Met</sup></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Scenedesmus obliquus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">7 days</td><td align="center" valign="middle" rowspan="1" colspan="1">20 µg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">534% stimulation *</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B37-ijms-16-23929" ref-type="bibr">37</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">V <sup>Met</sup></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella pyrenoidosa</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">7 days</td><td align="center" valign="middle" rowspan="1" colspan="1">1 µg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">67% stimulation</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B38-ijms-16-23929" ref-type="bibr">38</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">V <sup>Met</sup></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella pyrenoidosa</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">7 days</td><td align="center" valign="middle" rowspan="1" colspan="1">>1 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibitory threshold</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B38-ijms-16-23929" ref-type="bibr">38</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">V <sup>Ort</sup></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Haematococcus lacustris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">4 days</td><td align="center" valign="middle" rowspan="1" colspan="1">2.5–5 mM</td><td align="center" valign="middle" rowspan="1" colspan="1">Full inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B39-ijms-16-23929" ref-type="bibr">39</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">V <sup>Oxi</sup></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Scenedesmus quadricauda</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">12 days</td><td align="center" valign="middle" rowspan="1" colspan="1">2.23 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B40-ijms-16-23929" ref-type="bibr">40</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Ce</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Desmodesmus quadricauda</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">3 days</td><td align="center" valign="middle" rowspan="1" colspan="1">6 µmol/L</td><td align="center" valign="middle" rowspan="1" colspan="1">16% stimulation <italic><sup>A</sup></italic></td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B41-ijms-16-23929" ref-type="bibr">41</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Ce</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Desmodesmus quadricauda</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">3 days</td><td align="center" valign="middle" rowspan="1" colspan="1">94 µmol/L</td><td align="center" valign="middle" rowspan="1" colspan="1">~19% inhibition <italic><sup>A</sup></italic></td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B41-ijms-16-23929" ref-type="bibr">41</xref>]</td></tr><tr><td rowspan="2" align="center" valign="middle" colspan="1">Ce</td><td rowspan="2" align="center" valign="middle" colspan="1"><italic>Desmodesmus quadricauda</italic></td><td rowspan="2" align="center" valign="middle" colspan="1">3 days</td><td rowspan="2" align="center" valign="middle" colspan="1">5.74 µmol/L</td><td align="center" valign="middle" rowspan="1" colspan="1">20% inhibition <italic><sup>B</sup></italic></td><td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B41-ijms-16-23929" ref-type="bibr">41</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">60% stimulation <italic><sup>C</sup></italic></td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Ce</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Desmodesmus quadricauda</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">3 days</td><td align="center" valign="middle" rowspan="1" colspan="1">1.14 µmol/L</td><td align="center" valign="middle" rowspan="1" colspan="1">40% inhibition <italic><sup>D</sup></italic></td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B41-ijms-16-23929" ref-type="bibr">41</xref>]</td></tr><tr><td rowspan="2" align="center" valign="middle" colspan="1">Ce</td><td rowspan="2" align="center" valign="middle" colspan="1"><italic>Anabaena flosaquae</italic></td><td rowspan="2" align="center" valign="middle" colspan="1">17 days</td><td align="center" valign="middle" rowspan="1" colspan="1">0.1 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">~16% stimulation</td><td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B27-ijms-16-23929" ref-type="bibr">27</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">5–10 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">~33% inhibition</td></tr><tr><td rowspan="2" align="center" valign="middle" colspan="1">La</td><td rowspan="2" align="center" valign="middle" colspan="1"><italic>Desmodesmus quadricauda</italic></td><td rowspan="2" align="center" valign="middle" colspan="1">3 days</td><td rowspan="2" align="center" valign="middle" colspan="1">5.72 µmol/L</td><td align="center" valign="middle" rowspan="1" colspan="1">10% inhibition <italic><sup>B</sup></italic></td><td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B41-ijms-16-23929" ref-type="bibr">41</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">80% stimulation <italic><sup>C</sup></italic></td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">La</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Desmodesmus quadricauda</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">3 days</td><td align="center" valign="middle" rowspan="1" colspan="1">1.13 µmol/L</td><td align="center" valign="middle" rowspan="1" colspan="1">No change <italic><sup>D</sup></italic></td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B41-ijms-16-23929" ref-type="bibr">41</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">La</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Scenedesmus quadricauda</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">22–23 days</td><td align="center" valign="middle" rowspan="1" colspan="1">72 µmol/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B42-ijms-16-23929" ref-type="bibr">42</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">La, Ce, Nd, Sm, Eu, Gd, Tb, Dy, Ho, Er, Tm, Yb, Lu</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Skeletonema costatum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">96 h</td><td align="center" valign="middle" rowspan="1" colspan="1">28–29 µmol/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B43-ijms-16-23929" ref-type="bibr">43</xref>]</td></tr><tr><td rowspan="2" align="center" valign="middle" colspan="1">Nd</td><td rowspan="2" align="center" valign="middle" colspan="1"><italic>Desmodesmus quadricauda</italic></td><td rowspan="2" align="center" valign="middle" colspan="1">3 days</td><td rowspan="2" align="center" valign="middle" colspan="1">5.76 µmol/L</td><td align="center" valign="middle" rowspan="1" colspan="1">10% stimulation <italic><sup>B</sup></italic></td><td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B41-ijms-16-23929" ref-type="bibr">41</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">120% stimulation <italic><sup>C</sup></italic></td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Nd</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Desmodesmus quadricauda</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">3 days</td><td align="center" valign="middle" rowspan="1" colspan="1">1.09 µmol/L</td><td align="center" valign="middle" rowspan="1" colspan="1">~5% inhibition <italic><sup>D</sup></italic></td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B41-ijms-16-23929" ref-type="bibr">41</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">TiO<sub>2</sub>-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Nitzschia closterium</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">96 h</td><td align="center" valign="middle" rowspan="1" colspan="1">88–118 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B49-ijms-16-23929" ref-type="bibr">49</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">TiO<sub>2</sub>-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pseudokirchneriella subcapitata</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">2.53 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B52-ijms-16-23929" ref-type="bibr">52</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">TiO<sub>2</sub>-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">–</td><td align="center" valign="middle" rowspan="1" colspan="1">2.5–5 g/L</td><td align="center" valign="middle" rowspan="1" colspan="1">42% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B74-ijms-16-23929" ref-type="bibr">74</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">ZnO-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">200 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">35% cell viability</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B50-ijms-16-23929" ref-type="bibr">50</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">ZnO-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Dunaliella tertiolecta</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">96 h</td><td align="center" valign="middle" rowspan="1" colspan="1">2.4 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B56-ijms-16-23929" ref-type="bibr">56</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">ZnO-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pseudokirchneriella subcapitata</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">0.1 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">80% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B52-ijms-16-23929" ref-type="bibr">52</xref>]</td></tr><tr><td rowspan="3" align="center" valign="middle" colspan="1">ZnO-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Phaeodactylum tricornutum</italic></td><td rowspan="3" align="center" valign="middle" colspan="1">–</td><td align="center" valign="middle" rowspan="1" colspan="1">100 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">80% inhibition</td><td rowspan="3" align="center" valign="middle" colspan="1">[<xref rid="B51-ijms-16-23929" ref-type="bibr">51</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Alexandrium minutum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">100 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">80% inhibition</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Tetraselmis suecica</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">100 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">No effect</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">ZnO-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Scenedesmus rubescens</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">96 h </td><td align="center" valign="middle" rowspan="1" colspan="1">14.27 mg/L or >810 mg/L <sup>CM</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B53-ijms-16-23929" ref-type="bibr">53</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">CeO<sub>2</sub>-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pseudokirchneriella subcapitata</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">4.1–6.2 mg/L <sup>AS</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B55-ijms-16-23929" ref-type="bibr">55</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NiO-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">120 h</td><td align="center" valign="middle" rowspan="1" colspan="1">44 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B75-ijms-16-23929" ref-type="bibr">75</xref>]</td></tr><tr><td rowspan="3" align="center" valign="middle" colspan="1">Y<sub>2</sub>O<sub>3</sub>-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Phaeodactylum tricornutum</italic></td><td rowspan="3" align="center" valign="middle" colspan="1">–</td><td align="center" valign="middle" rowspan="1" colspan="1">100 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">~40% inhibition</td><td rowspan="3" align="center" valign="middle" colspan="1">[<xref rid="B51-ijms-16-23929" ref-type="bibr">51</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Alexandrium minutum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">100 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">~40% inhibition</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Tetraselmis suecica</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">100 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">70% inhibition</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">BaTiO<sub>3</sub>-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">1 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">~57% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B76-ijms-16-23929" ref-type="bibr">76</xref>]</td></tr><tr><td rowspan="2" align="center" valign="middle" colspan="1">Al<sub>2</sub>O<sub>3</sub>-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">45.4 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td rowspan="2" align="center" valign="middle" colspan="1">[<xref rid="B54-ijms-16-23929" ref-type="bibr">54</xref>] </td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Scenedesmus</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">39.35 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Ag-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pseudokirchneriella subcapitata</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">1.63 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B77-ijms-16-23929" ref-type="bibr">77</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Pt-NPs</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pseudokirchneriella subcapitata</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">72 h</td><td align="center" valign="middle" rowspan="1" colspan="1">16.9 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">50% inhibition</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B77-ijms-16-23929" ref-type="bibr">77</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">nZVI-Nanofer 25</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Arthrospira maxima</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">216 h</td><td align="center" valign="middle" rowspan="1" colspan="1">5.1 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">19% stimulation</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B57-ijms-16-23929" ref-type="bibr">57</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">nZVI-Nanofer 25</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Desmodesmus subspicatus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">216 h</td><td align="center" valign="middle" rowspan="1" colspan="1">5.1 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">73% stimulation</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B57-ijms-16-23929" ref-type="bibr">57</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nZVI-Nanofer 25</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Parachlorella kessleri</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">216 h</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">5.1 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">38% stimulation</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B57-ijms-16-23929" ref-type="bibr">57</xref>]</td></tr></tbody></table><table-wrap-foot><p>MMC, Minimum Metal Concentration significantly affecting Chlorophyll a intensity; <sup>T</sup>, depending on temperature applied; <sup>+</sup>, depending on Cd salt used; <sup>x</sup>, including complex abilities of media mineral elements; *, when compared to <italic>Scenedesmus</italic> growth in Fe deficient medium; <sup>ZnL</sup>, at low Zn concentrations; <sup>Met</sup>, added as metavanadate; <sup>Ort</sup>, added as orthovanadate; <sup>Oxi</sup>, added as vanadium pentoxide; <italic><sup>A</sup></italic>, in standard medium and compared to a control in standard medium without Ce; <italic><sup>B</sup></italic>, in Ca deficient medium and compared to a control in standard medium without tested metal; <italic><sup>C</sup></italic>, in Ca deficient medium and compared to a control in Ca deficient medium without tested metal; <italic><sup>D</sup></italic>, in Mn deficient medium and compared to a control in Mn deficient medium without tested metal; NPs, nanoparticles; <sup>CM</sup>, depending on culture medium; <sup>AS</sup>, depending on aged suspension; nZVI, zero-valent iron nanoparticles; Ref., Reference.</p></table-wrap-foot></table-wrap></sec><sec id="sec3-ijms-16-23929"><title>3. Metal Stress as a Method for Stimulation of Bioproduct Synthesis</title><p>Accumulation of metals in microalgae cells consists of two mechanisms: metal adsorption on the cell wall surface containing functional groups (carboxyl, hydroxyl, phosphate, amino, sulfhydryl) and absorption of metals inside cells via metal transport systems [<xref rid="B12-ijms-16-23929" ref-type="bibr">12</xref>,<xref rid="B19-ijms-16-23929" ref-type="bibr">19</xref>,<xref rid="B78-ijms-16-23929" ref-type="bibr">78</xref>]. Metals in microalgae cells can cause formation of reactive oxygen species (ROS) such as hydroxyl radical (·OH), superoxide anion (O<sub>2</sub>·<sup>−</sup>), singlet oxygen (O<sub>2</sub>*) and hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>) that interact with lipids, proteins and nucleic acids, resulting in their degradation. As a protective response to metal induced oxidative stress, microalgae cells synthetize chelating agents such as phytochelatin or exopolymers in higher amounts [<xref rid="B12-ijms-16-23929" ref-type="bibr">12</xref>,<xref rid="B79-ijms-16-23929" ref-type="bibr">79</xref>,<xref rid="B80-ijms-16-23929" ref-type="bibr">80</xref>]. Chelating agents are organic compounds that form two or more bonds with a metal ion, thereby creating a coordination complex chelate–metal and preventing metal ions from interaction with biological macromolecules [<xref rid="B81-ijms-16-23929" ref-type="bibr">81</xref>]. Another defense mechanism againsts oxidative stress is the synthesis of antioxidant compounds (pigments, glutathione, ascorbate) or enzymes (superoxide dismutase, catalase) that are responsible for quenching reactive oxygen species (ROS) and also reducing metal ions into their less reactive forms [<xref rid="B12-ijms-16-23929" ref-type="bibr">12</xref>,<xref rid="B79-ijms-16-23929" ref-type="bibr">79</xref>,<xref rid="B80-ijms-16-23929" ref-type="bibr">80</xref>]. Therefore, oxidative stress can be considered as a trigger mechanism to induce production of target compounds by metal-exposed microalgae cells, under conditions where the detrimental effect of metals on microalgal culture is avoided.</p><sec id="sec3dot1-ijms-16-23929"><title>3.1. Pigments</title><p>Chlorophylls, carotenoids and phycobilins are microalgal pigments that harvest light in the process of photosynthesis. Chlorophylls are primary photosynthic pigments that contain tetrapyrrole macrocycle rings and are present in various forms (a, b, c1, c2, c3, d, f), in different microalgae or cyanobacteria species (<xref ref-type="table" rid="ijms-16-23929-t002">Table 2</xref>). Green microalgae possess chlorophyll content up to 6.7% [<xref rid="B82-ijms-16-23929" ref-type="bibr">82</xref>], and upon chemical modifications, to phaeophytin [<xref rid="B83-ijms-16-23929" ref-type="bibr">83</xref>] or Cu<sup>2+</sup>-chlorophyllin [<xref rid="B84-ijms-16-23929" ref-type="bibr">84</xref>], can be used as a biomordant [<xref rid="B83-ijms-16-23929" ref-type="bibr">83</xref>] to enchance the dyeing process of textile products or as a textile dye [<xref rid="B84-ijms-16-23929" ref-type="bibr">84</xref>] with antimicrobial properties. Additionally, an Mg<sup>2+</sup> ion in a chlorophyll centre can be substituted with Zn<sup>2+</sup>, Ni<sup>2+</sup>, Cd<sup>2+</sup>, Pb<sup>2+</sup>, Co<sup>2+</sup> or Pt<sup>2+</sup> [<xref rid="B85-ijms-16-23929" ref-type="bibr">85</xref>,<xref rid="B86-ijms-16-23929" ref-type="bibr">86</xref>,<xref rid="B87-ijms-16-23929" ref-type="bibr">87</xref>,<xref rid="B88-ijms-16-23929" ref-type="bibr">88</xref>,<xref rid="B89-ijms-16-23929" ref-type="bibr">89</xref>,<xref rid="B90-ijms-16-23929" ref-type="bibr">90</xref>]. Carotenoids–accessory photosynthetic pigments, are fat-soluble tetraterpenoid molecules that are divided into no oxygen-containing carotenes (β-carotene) and oxygen-containing xanthophylls (lutein, astaxanthin, zeaxanthin) [<xref rid="B91-ijms-16-23929" ref-type="bibr">91</xref>]. Phycobiliproteins are water-soluble proteins that serve as accessory pigments in blue-green or red microalgae, giving a blue (c-phycocyanin, allophycocyanin) [<xref rid="B34-ijms-16-23929" ref-type="bibr">34</xref>,<xref rid="B92-ijms-16-23929" ref-type="bibr">92</xref>] or pink, red (b-phycoerythrin, c-phycoerythrin) [<xref rid="B93-ijms-16-23929" ref-type="bibr">93</xref>,<xref rid="B94-ijms-16-23929" ref-type="bibr">94</xref>] colour. Chlorophylls, carotenoids and Phycobiliproteins can find applications in food, cosmetic and pharmaceutical products as coloring, antioxidant, food additive or therapeutic agents [<xref rid="B95-ijms-16-23929" ref-type="bibr">95</xref>,<xref rid="B96-ijms-16-23929" ref-type="bibr">96</xref>,<xref rid="B97-ijms-16-23929" ref-type="bibr">97</xref>].</p><table-wrap id="ijms-16-23929-t002" position="float"><object-id pub-id-type="pii">ijms-16-23929-t002_Table 2</object-id><label>Table 2</label><caption><p>Types of chlorophyll present in eukaryotic microalgae and cyanobacteria.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Chlorophyll Type</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Microalgae Strain</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Taxonomy</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">a, b</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Green microalgae</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B98-ijms-16-23929" ref-type="bibr">98</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">a, c1, c2</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Phaeodactylum tricornutum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Diatoms</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B99-ijms-16-23929" ref-type="bibr">99</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">a, c1, c2</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Kryptoperidinium foliaceum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Dinoflagellates</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B100-ijms-16-23929" ref-type="bibr">100</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">a, c2, c3</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Karenia mikimotoi</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Dinoflagellates</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B100-ijms-16-23929" ref-type="bibr">100</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">a, d</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Acaryochloris marina</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Cyanobacteria</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B101-ijms-16-23929" ref-type="bibr">101</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">a, f</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Halomicronema hongdechloris</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cyanobacteria</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B102-ijms-16-23929" ref-type="bibr">102</xref>]</td></tr></tbody></table></table-wrap><p>The presence of metals can have an enchancing effect on pigment content in microalgae or cyanobacteria cells. Copper (Cu<sup>2+</sup>) at concentration between 0.05–0.2 g/L induced β-carotene production in <italic>Chlamydomonas acidophilla</italic> [<xref rid="B103-ijms-16-23929" ref-type="bibr">103</xref>]. The change in iron (Fe<sup>2+</sup>) medium concentation resulted in a growth improvement and an increase in lutein, zeaxanthin and β-carotene content in <italic>Coccomyxa onubensis</italic> cells [<xref rid="B104-ijms-16-23929" ref-type="bibr">104</xref>]. Also, β-carotene content in <italic>Dunaliella salina</italic> cells was increased seven times in the presence of 450 µM Fe<sup>2+</sup> and 67.5 mM acetate, however at the expense of four-fold reduction in <italic>Dunaliella</italic> cell number [<xref rid="B105-ijms-16-23929" ref-type="bibr">105</xref>]. Cyanobacterium <italic>Nostoc minutum</italic> cultivated photoautotrophically in medium containg 1 g/L arsenic(V) was reported to posses chlorophyll, carotenoid and allophycocyanin content higher by 75%, 40% and 25%, respectively, when compared to control culture [<xref rid="B34-ijms-16-23929" ref-type="bibr">34</xref>]. Similarly, small concentrations of Ni (0.1–10 µM) increased chlorophyll content and c-phycocyanin production even by 47% and up to 4.35 times, respectively, in <italic>Anabaena</italic><italic>doliolum</italic> culture [<xref rid="B92-ijms-16-23929" ref-type="bibr">92</xref>]. The content of c-phycocyanin, phycoerythrin and allophycocyanin in cyanobacterium <italic>Phormidium tenue</italic> culture increased considerably in the presence of As, but the uplift profiles were strongly dependent on As dosage (0.1–100 ppm) and exposure time [<xref rid="B106-ijms-16-23929" ref-type="bibr">106</xref>]. In other studies, cultivation of <italic>Synechocystis</italic> sp. in the presence of Pb and Cd, and <italic>Spirulina platensis</italic> in the presence of Pb, showed a decrease in biomass and pigment (chlorophyll, carotenoid, phycocyanin) concentration, in the culture volume. Nevertheless, pigment content in cyanobacteria biomass increased at some metal concentrations and cyanobacteria growth was stimulated at low Pb concentrations [<xref rid="B107-ijms-16-23929" ref-type="bibr">107</xref>,<xref rid="B108-ijms-16-23929" ref-type="bibr">108</xref>]. Lead (Pb) and cadmium (Cd) at concentrations up to 10 mg/L increased chlorophyll concentration in cultures of metal resistant <italic>Scenedesmus quadricauda</italic> and <italic>Pseudochlorococcum typicum</italic> [<xref rid="B109-ijms-16-23929" ref-type="bibr">109</xref>]. Tellurium (TeO<sub>3</sub><sup>2−</sup>), added into <italic>Spirulina platensis</italic> growth media, was accumulated and incorporated into peptides in <italic>Spirulina</italic> cells. As a result, production of Te-phycocyanin and Te-allophycocyanin possessing enhanced antioxidant activity, was reported in <italic>Spirulina platensis</italic> cells [<xref rid="B110-ijms-16-23929" ref-type="bibr">110</xref>].</p></sec><sec id="sec3dot2-ijms-16-23929"><title>3.2. Lipids</title><p>Microalgal cells are a source of lipids including triacyloglycerols (TAGs) and fatty acids [<xref rid="B111-ijms-16-23929" ref-type="bibr">111</xref>], but also phytosterols [<xref rid="B112-ijms-16-23929" ref-type="bibr">112</xref>] and sphingolipids [<xref rid="B113-ijms-16-23929" ref-type="bibr">113</xref>], with potential applications as biofuels, nutraceuticals and food additives. It is reported that nutrient deficiency such as nitrogen deprivation results in oxidative stress and lipid accumulation in microalgal cells [<xref rid="B114-ijms-16-23929" ref-type="bibr">114</xref>]. Cultivation of <italic>Chlorella minutissima</italic> in the presence of Cd (0.2–0.4 mM) or Cu (0.2–1 mM) leads to the increase in both biomass density and cell lipid content, providing lipid productivity improved 2.17-fold with 0.4 mM Cd or by 34% with 0.4 mM Cu [<xref rid="B115-ijms-16-23929" ref-type="bibr">115</xref>]. <italic>Euglena gracilis</italic> cultivated photoautotrophically or mixotrophically in the presence of low chromium (Cr<sup>6+</sup>) concentration exhibited higher total lipid content, although lipid stimulation (10%–100%) was dependent on <italic>Euglena</italic> strain used and medium composition tested [<xref rid="B116-ijms-16-23929" ref-type="bibr">116</xref>]. Addition of 0.1 g/L TiO<sub>2</sub> nanoparticles with UV-A irradiation applied, slightly increased production of fatty acids in <italic>Chlorella vulgaris</italic> cells, without growth reduction [<xref rid="B74-ijms-16-23929" ref-type="bibr">74</xref>]. Recently, zero-valent iron nanoparticles (5.1 mg/L) were reported to increase lipid productivity in <italic>Arthrospira maxima</italic>, <italic>Desmodesmus subspicatus</italic> and <italic>Parachlorella kessleri</italic> cultures, respectively by 40%, 2.75-fold and by 66% [<xref rid="B57-ijms-16-23929" ref-type="bibr">57</xref>]. Metal stress also causes the alteration of fatty acid profile in microalgae cells. The effect of As(III) on <italic>Nannochloropsis</italic> sp. cells resulted in a slight increase in cell lipid content and a change in lipid profile, as the decrease in polyunsaturated fatty acids and the increase in short-chain saturated (C16:0, C18:0) and monounsaturated (C16:1, C18:1) fatty acids, was depicted [<xref rid="B117-ijms-16-23929" ref-type="bibr">117</xref>]. Nickel at 0.5 mg/L caused a shift of fatty acid profile towards saturated fatty acids (C14:0, C16:0, C20:0) in <italic>Dunaliella salina</italic> and <italic>Nannochloropsis salina</italic> cells, also with the upshift of saturated C18:0 and unsaturated C18:2 for <italic>Nannochloropsis</italic> and C22:0 behenic acid for <italic>Dunaliella</italic> [<xref rid="B118-ijms-16-23929" ref-type="bibr">118</xref>]. Composition of fatty acids (chain length, number of double bonds) defines the biodiesels produced from corresponding triglycerides in terms of their quality and properties (including cetane number, density, viscosity, lubricity, calorific value, NO<italic><sub>x</sub></italic> emissions) [<xref rid="B119-ijms-16-23929" ref-type="bibr">119</xref>,<xref rid="B120-ijms-16-23929" ref-type="bibr">120</xref>,<xref rid="B121-ijms-16-23929" ref-type="bibr">121</xref>]. Therefore, metal stress can be applied to alter composition of fatty acids in microalgal cells and produce biodiesel of desirable quality and properties [<xref rid="B117-ijms-16-23929" ref-type="bibr">117</xref>]. As a contrary, cultivation of <italic>Nannochloropsis limnetica</italic> and <italic>Trachydiscus minutus</italic> in the presence of zero-valent iron nanoparticles (nZVI) caused the decrease in saturated fatty acids (C14:0, C16:0, C18:0) and the increase in eicosapentaenoic acid (C20:5ω3) content in <italic>Nannochloropsis</italic> and <italic>Trachydiscus</italic> biomass [<xref rid="B57-ijms-16-23929" ref-type="bibr">57</xref>]. Eicosapentaenoic acid (EPA) can be used as a nutraceutical or pharmacological agent for the treatment of heart and inflammatory diseases [<xref rid="B122-ijms-16-23929" ref-type="bibr">122</xref>].</p></sec><sec id="sec3dot3-ijms-16-23929"><title>3.3. Exopolymers</title><p>Extracellular polymeric substances (EPS), consisting of exopolysaccharides and exoproteins, are excreted by microalgae and cyanobacteria upon exposure to stress factors such as nutrient (N, P) imbalance, but the release mechanism can also depend on cultivation conditions (light intensity, temperature, salinity, microelement availability) and the stage of microalgal growth [<xref rid="B123-ijms-16-23929" ref-type="bibr">123</xref>,<xref rid="B124-ijms-16-23929" ref-type="bibr">124</xref>,<xref rid="B125-ijms-16-23929" ref-type="bibr">125</xref>,<xref rid="B126-ijms-16-23929" ref-type="bibr">126</xref>,<xref rid="B127-ijms-16-23929" ref-type="bibr">127</xref>,<xref rid="B128-ijms-16-23929" ref-type="bibr">128</xref>]. Exopolysaccharides can be of linear or branched structure and contain C6 (glucose, galactose, fructose, rhamnose, fucose) and C5 (xylose, arabinose) sugars, as well as uronic (glucuronic, galacturonic) acids, aromatic, pyruvate, acetate, sulphate and halide groups. Additionally, extracellular polysaccharides can be also coupled with peptides, lipids and nucleic acids [<xref rid="B129-ijms-16-23929" ref-type="bibr">129</xref>,<xref rid="B130-ijms-16-23929" ref-type="bibr">130</xref>].</p><p>Metals were reported to stimulate the release of exopolymers by microalgal cells. A considerable increase in the release of exopolysaccharides and extracellullar proteins was observed in the culture of cyanobacterium <italic>Lyngbya putealis</italic>, as a response to the presence of Cu and Co [<xref rid="B131-ijms-16-23929" ref-type="bibr">131</xref>]. Increased release of extracellular polymers from <italic>Thalassiosira weissflogii</italic> [<xref rid="B132-ijms-16-23929" ref-type="bibr">132</xref>], and <italic>Thalassiosira pseudonana</italic> [<xref rid="B133-ijms-16-23929" ref-type="bibr">133</xref>] in the presence of Ag [<xref rid="B132-ijms-16-23929" ref-type="bibr">132</xref>] and Cd [<xref rid="B133-ijms-16-23929" ref-type="bibr">133</xref>] ions released from engineered nanoparticles (ENPs), was also reported. Extracellular polymeric substances possess antiviral, antitumor, anticoagulant, antiinflammatory and immunostimulant activity, but they can also serve as biosurfactants, biolubricants, bioemulsifiers [<xref rid="B130-ijms-16-23929" ref-type="bibr">130</xref>] and a source of sugars for biofuels [<xref rid="B134-ijms-16-23929" ref-type="bibr">134</xref>].</p></sec><sec id="sec3dot4-ijms-16-23929"><title>3.4. Phytochelatin</title><p>Phytochelatins are (oligo)peptides synthetized in plants, yeast, algae and cyanobacteria for detoxification of heavy metals. The structure of phytochelatin is (γ-Glu-Cys)<sub>n</sub>-Gly with γ-Glu-Cys <italic>n</italic> being between 2 to 11. Phytochelatin is synthetized by phytochelatin synthase (glutathione-γ-glutamylcysteinyltransferase), by firstly adding γ-Glu-Cys from glutathione (γ-Glu-Cys-Gly) to another glutathione molecule forming (γ-Glu-Cys)<sub>2</sub>-Gly (PC2) and further incorporates new γ-Glu-Cys units into PC2 [<xref rid="B135-ijms-16-23929" ref-type="bibr">135</xref>]. Synthesis of short chain phytochelatins (2 to 6 of γ-Glu-Cys units) was reported in cells of microalgae (Table 3) such as <italic>Scenedesmus vacuolatus</italic> [<xref rid="B136-ijms-16-23929" ref-type="bibr">136</xref>], <italic>Phaeodactylum tricornutum</italic> [<xref rid="B137-ijms-16-23929" ref-type="bibr">137</xref>,<xref rid="B138-ijms-16-23929" ref-type="bibr">138</xref>,<xref rid="B139-ijms-16-23929" ref-type="bibr">139</xref>], <italic>Scenedesmus armatus</italic> [<xref rid="B140-ijms-16-23929" ref-type="bibr">140</xref>], <italic>Stichococcus bacillaris</italic> [<xref rid="B141-ijms-16-23929" ref-type="bibr">141</xref>], <italic>Micrasterias denticulata</italic> [<xref rid="B142-ijms-16-23929" ref-type="bibr">142</xref>] and cyanobacterium <italic>Anabaena doliolum</italic> [<xref rid="B143-ijms-16-23929" ref-type="bibr">143</xref>] exposed to increasing concentration of Cd, Pb, Cu and/or As. Phytochelatin content in <italic>Scenedesmus armatus</italic> and <italic>Stichococcus bacillaris</italic> cells exposed to constant (Const.) concentration of Cd and As respectively can be also further elevated, with the upshift of CO<sub>2</sub> supplementation for <italic>Scenedesmus</italic> [<xref rid="B140-ijms-16-23929" ref-type="bibr">140</xref>] and decrease of pH for <italic>Stichococcus</italic> [<xref rid="B141-ijms-16-23929" ref-type="bibr">141</xref>]. Also synthesis of iso-phytochelatins such as Cys(GluCys)<italic><sub>n</sub></italic>Gly and (GluCys)<italic><sub>n</sub></italic>Ala was reported in <italic>Chlamydomonas reinhardtii</italic> upon Cd exposure [<xref rid="B144-ijms-16-23929" ref-type="bibr">144</xref>]. Phytochelatins, obtained from microalgae cultures, can become a component for biosensors, designed for detection of heavy metals in samples of environmental, biological or pharmaceutical origin [<xref rid="B145-ijms-16-23929" ref-type="bibr">145</xref>,<xref rid="B146-ijms-16-23929" ref-type="bibr">146</xref>].</p><table-wrap id="ijms-16-23929-t003" position="float"><object-id pub-id-type="pii">ijms-16-23929-t003_Table 3</object-id><label>Table 3</label><caption><p>Synthesis of phytochelatin in microalgae exposed to heavy metals.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Strain</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Metal</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Metal Uplift</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Phytochelatin Uplift</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">PCN <sup>A</sup></th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Growth Rate <sup>C</sup></th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Scenedesmus vacuolatus</italic></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Cd</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">0.3→79 nM</td><td align="center" valign="middle" rowspan="1" colspan="1">~3→25 amol/cell</td><td align="center" valign="middle" rowspan="1" colspan="1">PC2</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Reduced by 37%</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B136-ijms-16-23929" ref-type="bibr">136</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">~1→44 amol/cell</td><td align="center" valign="middle" rowspan="1" colspan="1">PC3</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~0→17 amol/cell</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PC4</td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Phaeodactylum tricornutum</italic></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Cd</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">0→0.45 µM</td><td align="center" valign="middle" rowspan="1" colspan="1">~0.16→3.6 amol/cell</td><td align="center" valign="middle" rowspan="1" colspan="1">PC2</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">No change</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B137-ijms-16-23929" ref-type="bibr">137</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">~0.5→1.3 amol/cell</td><td align="center" valign="middle" rowspan="1" colspan="1">PC3</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~0.05→1.5 amol/cell</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PC4</td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Phaeodactylum tricornutum</italic></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Cu</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">0.068 pM→0.4 µM</td><td align="center" valign="middle" rowspan="1" colspan="1">~0.16→1.7 amol/cell</td><td align="center" valign="middle" rowspan="1" colspan="1">PC2</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">No change</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B137-ijms-16-23929" ref-type="bibr">137</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">~0.5→1.5 amol/cell</td><td align="center" valign="middle" rowspan="1" colspan="1">PC3</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~0.05→0.8 amol/cell</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PC4</td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Phaeodactylum tricornutum</italic></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Cd</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">0→10 µM</td><td align="center" valign="middle" rowspan="1" colspan="1">~0→12.5 amol/cell</td><td align="center" valign="middle" rowspan="1" colspan="1">PC2</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Toxic effect avoided</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B138-ijms-16-23929" ref-type="bibr">138</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">~0→25 amol/cell</td><td align="center" valign="middle" rowspan="1" colspan="1">PC4</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~0→5 amol/cell</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PC5</td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Phaeodactylum tricornutum</italic></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Pb</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">0→10 µM</td><td align="center" valign="middle" rowspan="1" colspan="1">~0→50 amol/cell</td><td align="center" valign="middle" rowspan="1" colspan="1">PC2</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Toxic effect avoided</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B138-ijms-16-23929" ref-type="bibr">138</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">~0→13 amol/cell</td><td align="center" valign="middle" rowspan="1" colspan="1">PC3</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~0→3 amol/cell</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PC5</td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Phaeodactylum tricornutum</italic></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Cu</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">0→10 µM</td><td align="center" valign="middle" rowspan="1" colspan="1">~2→18 amol/cell</td><td align="center" valign="middle" rowspan="1" colspan="1">PC2</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">–</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B139-ijms-16-23929" ref-type="bibr">139</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">~0→38 amol/cell</td><td align="center" valign="middle" rowspan="1" colspan="1">PC3</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~0→5 amol/cell</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PC6</td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Scenedesmus armatus</italic></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Cd</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Const. 93 µM *</td><td align="center" valign="middle" rowspan="1" colspan="1">~40→200 nmol-SH/g</td><td align="center" valign="middle" rowspan="1" colspan="1">PC2</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Reduced by 26%</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B140-ijms-16-23929" ref-type="bibr">140</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">~80→1300 nmol-SH/g</td><td align="center" valign="middle" rowspan="1" colspan="1">PC3</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~20→280 nmol-SH/g</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PC4</td></tr><tr><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Stichococcus bacillaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">As(III)</td><td align="center" valign="middle" rowspan="1" colspan="1">Const. 100 µM **</td><td align="center" valign="middle" rowspan="1" colspan="1">0.07→0.15 µmol-SH/g</td><td align="center" valign="middle" rowspan="1" colspan="1">PC2</td><td align="center" valign="middle" rowspan="1" colspan="1">Reduced by 20%</td><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B141-ijms-16-23929" ref-type="bibr">141</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">As(V)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Const. 100 µM **</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0.14→0.38 µmol-SH/g</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PC2</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Reduced by 30%</td></tr></tbody></table><table-wrap-foot><fn><p><sup>A</sup> Phytochelatin with N number of γGlu-Cys units; <sup>C</sup> when compared to control; * increase of CO<sub>2</sub> supplementation from 0.1% to 2%; ** pH shift from 8.2 to 6.8.</p></fn></table-wrap-foot></table-wrap></sec><sec id="sec3dot5-ijms-16-23929"><title>3.5. Phytohormones</title><p>Zeatin, indoleacetic acid and abscisic acid are phytohormones that can be used as growth regulators for plants [<xref rid="B147-ijms-16-23929" ref-type="bibr">147</xref>,<xref rid="B148-ijms-16-23929" ref-type="bibr">148</xref>], and yeast [<xref rid="B149-ijms-16-23929" ref-type="bibr">149</xref>], but also as anti-aging agents [<xref rid="B150-ijms-16-23929" ref-type="bibr">150</xref>] and potential drugs for neural [<xref rid="B151-ijms-16-23929" ref-type="bibr">151</xref>] or cancer [<xref rid="B152-ijms-16-23929" ref-type="bibr">152</xref>] diseases. Phytohormones can be found in microalgae [<xref rid="B153-ijms-16-23929" ref-type="bibr">153</xref>] and their content can be amplified in the presence of heavy metals. The content of indoleacetic acid, zeatin and abscisic acid increased in <italic>Chlorella vulgaris</italic> cells grown in the medium containing 10<sup>−4</sup> M Cd, Pb or Cu, however at the expense of decreased cell number in the culture. Interestingly, addition of 10<sup>−8</sup> M brassinolide into metal-containing <italic>Chlorella</italic> culture enabled to achieve cell number comparable to control culture, together with further stimulation of zeatin, indoleacetic acid and abscisic acid production [<xref rid="B154-ijms-16-23929" ref-type="bibr">154</xref>].</p></sec><sec id="sec3dot6-ijms-16-23929"><title>3.6. Organoarsenical Compounds</title><p>Accumulation of As in microalgae cells has been recently extensively summarized [<xref rid="B155-ijms-16-23929" ref-type="bibr">155</xref>]. In essence, the uptake of As(V) from surroundings into microalgae cells is accomplished by means of phosphate transport system, while As(III) is transported by aquaglyceroporins and hexose permeases [<xref rid="B155-ijms-16-23929" ref-type="bibr">155</xref>]. Subsequently, As(V) is reduced to As(III) via As reductase action, with simultaneous oxidation of glutathione (GSH). As(III) undergoes methylation via As methyltransferase action into monomethylarsonate (MMA) and dimethylarsinate (DMA). Arsenic(III) can also undergo bio-oxidation to As(V) or be extruded from cells [<xref rid="B156-ijms-16-23929" ref-type="bibr">156</xref>,<xref rid="B157-ijms-16-23929" ref-type="bibr">157</xref>,<xref rid="B158-ijms-16-23929" ref-type="bibr">158</xref>]. Arsenic(V) can be incorporated into cellular components such as sugars and lipids. In microalgae, dimethylarsinate (or its reduced form: dimethylarsinous acid) can combine with the adenosyl group from <italic>S</italic>-adenosyl methionine, leading to formation of a dimethylarsinyladenosine, which further undergoes glycosidation to dimethylarsenoribosides [<xref rid="B159-ijms-16-23929" ref-type="bibr">159</xref>,<xref rid="B160-ijms-16-23929" ref-type="bibr">160</xref>]. In cyanobacteria, dimethylarsinate undergoes reduction, ribose-coupling and glycosidation [<xref rid="B161-ijms-16-23929" ref-type="bibr">161</xref>]. Some varieties of arsenosugars containing glycerol, sulphate, sulphonate and phosphate groups were detected for microalgae [<xref rid="B160-ijms-16-23929" ref-type="bibr">160</xref>,<xref rid="B162-ijms-16-23929" ref-type="bibr">162</xref>]. Arsenolipids in microalgae were determined as dimethylarsenoriboside phospholipids (<xref ref-type="fig" rid="ijms-16-23929-f001">Figure 1</xref>), although phospholipids containing single As(V) or DMA groups were also reported [<xref rid="B163-ijms-16-23929" ref-type="bibr">163</xref>]. Content and compositions of arsenoorganics formed in microalgae <italic>Chlorella</italic> and <italic>Monoraphidium</italic> [<xref rid="B65-ijms-16-23929" ref-type="bibr">65</xref>], <italic>Dunaliella</italic> and <italic>Phaeodactylum</italic> [<xref rid="B163-ijms-16-23929" ref-type="bibr">163</xref>], <italic>Chlamydomonas</italic> [<xref rid="B160-ijms-16-23929" ref-type="bibr">160</xref>] or cyanobacteria <italic>Synechocystis</italic> [<xref rid="B157-ijms-16-23929" ref-type="bibr">157</xref>,<xref rid="B161-ijms-16-23929" ref-type="bibr">161</xref>] and <italic>Nostoc</italic> [<xref rid="B161-ijms-16-23929" ref-type="bibr">161</xref>] cells depends on microalgae strain used, as well as on arsenic(V) concentration applied, exposure time and phosphate availability. Arsenolipids and arsenosugars are currently evaluated as possible therapeutic agents [<xref rid="B164-ijms-16-23929" ref-type="bibr">164</xref>]. However, application of As-containing compounds is limited due to high toxicity and so far, only derivatives of arsenolipids have been reported to possess any medical applications [<xref rid="B159-ijms-16-23929" ref-type="bibr">159</xref>].</p><fig id="ijms-16-23929-f001" position="float"><label>Figure 1</label><caption><p>Chemical structure of dimethylarsenoriboside phospholipids (R—a carbon chain of fatty acid).</p></caption><graphic xlink:href="ijms-16-23929-g001"></graphic></fig></sec><sec id="sec3dot7-ijms-16-23929"><title>3.7. Nanoparticles and Nano-Needles</title><p>Nanoparticles are particles with sizes ranging between 1–100 nm [<xref rid="B165-ijms-16-23929" ref-type="bibr">165</xref>]. Nanoparticles possess antiviral, antibacterial, antifungal, anticancer and antiparasite activity. They also find application in the field of catalysis or photonics or can serve as drug carriers and components of chemical sensors [<xref rid="B166-ijms-16-23929" ref-type="bibr">166</xref>]. Methods applied for manufacturing nanoparticles range from mechanical, laser and UV irradiation treatment to microemulsion system, hydrothermal process, sol–gel process, chemical vapor condensation, sonochemical treatment and microbial biosynthesis [<xref rid="B165-ijms-16-23929" ref-type="bibr">165</xref>,<xref rid="B167-ijms-16-23929" ref-type="bibr">167</xref>]. Synthesis of nanoparticles by microorganisms (bacteria, yeast, fungi and microalgae) can constitute a green and environmentally friendly method for nanoparticles production [<xref rid="B168-ijms-16-23929" ref-type="bibr">168</xref>,<xref rid="B169-ijms-16-23929" ref-type="bibr">169</xref>]. Formation of nanoparticles: Au, Ag or Pd (<xref ref-type="table" rid="ijms-16-23929-t004">Table 4</xref>) from metal ions solutions takes place inside microalgae cells (intracellularly) or in the media (extracellularly) via interactions with molecules of microalgal cell metabolism (NADH, pigments, peptides, proteins and polysaccharides) [<xref rid="B170-ijms-16-23929" ref-type="bibr">170</xref>,<xref rid="B171-ijms-16-23929" ref-type="bibr">171</xref>,<xref rid="B172-ijms-16-23929" ref-type="bibr">172</xref>,<xref rid="B173-ijms-16-23929" ref-type="bibr">173</xref>,<xref rid="B174-ijms-16-23929" ref-type="bibr">174</xref>,<xref rid="B175-ijms-16-23929" ref-type="bibr">175</xref>,<xref rid="B176-ijms-16-23929" ref-type="bibr">176</xref>]. The size of synthetized nanoparticles depends on microalgal strain and metal type used, but place of synthesis, initial metal loading, light and temperature are also crucial factors influencing formation of nanoparticles. Additionally, synthesis of Cd nanoparticles in a form of CdS [<xref rid="B177-ijms-16-23929" ref-type="bibr">177</xref>] or Ni nanoparticles as a product of reduction of other nanoparticles (NiO) [<xref rid="B75-ijms-16-23929" ref-type="bibr">75</xref>], was also reported. Besides nanoparticles, biosynthesis of nanoneedles by microalgae also occurs; such nanoneedles, composed of zinc and phosphorous, were detected in <italic>Scenedesmus obliquus</italic> cells as a result of exposure to high Zn concentration [<xref rid="B178-ijms-16-23929" ref-type="bibr">178</xref>].</p><table-wrap id="ijms-16-23929-t004" position="float"><object-id pub-id-type="pii">ijms-16-23929-t004_Table 4</object-id><label>Table 4</label><caption><p>Synthesis of nanoparticles (NP) in microalgae and cyanobacteria cultures.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Element NP</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Source</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Strain</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Place of Synthesis</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Average Particle Size (nm)</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Gold (Au)</td><td align="center" valign="middle" rowspan="1" colspan="1">HAuCl<sub>4</sub>·3H<sub>2</sub>O</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Intracellularly</td><td align="center" valign="middle" rowspan="1" colspan="1">40–60</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B170-ijms-16-23929" ref-type="bibr">170</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Gold (Au)</td><td align="center" valign="middle" rowspan="1" colspan="1">KAuCl<sub>4</sub></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Eolimna minima</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Intracellularly</td><td align="center" valign="middle" rowspan="1" colspan="1">5–100</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B171-ijms-16-23929" ref-type="bibr">171</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Silver (Ag)</td><td align="center" valign="middle" rowspan="1" colspan="1">AgNO<sub>3</sub></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Parachlorella kessleri</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Extracellularly</td><td align="center" valign="middle" rowspan="1" colspan="1">9, 14 or 18</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B172-ijms-16-23929" ref-type="bibr">172</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Silver (Ag)</td><td align="center" valign="middle" rowspan="1" colspan="1">AgNO<sub>3</sub></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Botryococcus braunii</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Extracellularly</td><td align="center" valign="middle" rowspan="1" colspan="1">15.67</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B173-ijms-16-23929" ref-type="bibr">173</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Silver (Ag)</td><td align="center" valign="middle" rowspan="1" colspan="1">AgNO<sub>3</sub></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Scenedesmus</italic> sp.</td><td align="center" valign="middle" rowspan="1" colspan="1">Intracellularly</td><td align="center" valign="middle" rowspan="1" colspan="1">15–20</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B174-ijms-16-23929" ref-type="bibr">174</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Palladium (Pd)</td><td align="center" valign="middle" rowspan="1" colspan="1">Na<sub>2</sub>(PdCl<sub>4</sub>)</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Microalga culture</td><td align="center" valign="middle" rowspan="1" colspan="1">7</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B175-ijms-16-23929" ref-type="bibr">175</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Palladium (Pd)</td><td align="center" valign="middle" rowspan="1" colspan="1">PdCl<sub>2</sub></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Intracellularly</td><td align="center" valign="middle" rowspan="1" colspan="1">5–12</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B170-ijms-16-23929" ref-type="bibr">170</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Palladium (Pd)</td><td align="center" valign="middle" rowspan="1" colspan="1">PdCl<sub>2</sub></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Plectonema boryanum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Extracellularly</td><td align="center" valign="middle" rowspan="1" colspan="1">≤30</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B176-ijms-16-23929" ref-type="bibr">176</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Cadmium sulphide (CdS)</td><td align="center" valign="middle" rowspan="1" colspan="1">Cd(NO<sub>3</sub>)<sub>2</sub>·4H<sub>2</sub>O</td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Scenedesmus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Intracellularly</td><td align="center" valign="middle" rowspan="1" colspan="1">120–175 (described as nanoparticles)</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B177-ijms-16-23929" ref-type="bibr">177</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Nickel (Ni)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NiO–NPs</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Microalga culture</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">–</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B75-ijms-16-23929" ref-type="bibr">75</xref>]</td></tr></tbody></table></table-wrap></sec></sec><sec id="sec4-ijms-16-23929"><title>4. Influence of Growth Conditions on Microalgal Resistance Towards Metals</title><p>Metals at low concentration can be stimulatory for growth and production of target compounds, but metal overdose has detrimental and lethal effects on microalgae cultures. Hence, microalgal cultivation in metal polluted wastewaters should be designed in such a way to limit cell–metal interactions to the level at which metal concentration exerts only beneficial effects on microalgae growth and biosynthesis of crucial products. Microalgal cell response to metal presence depends on many factors such as conditions of cultivation, nutrient availability, presence of organic compounds and tolerance ability of particular strains.</p><sec id="sec4dot1-ijms-16-23929"><title>4.1. Growth Media Composition and Cultivation Conditions</title><p>Composition of growth media is a crucial factor regarding microalgae response towards heavy metals, such as arsenic, cadmium or nickel.</p><p>Arsenate (AsO<sub>4</sub><sup>3−</sup>) and phosphate (PO<sub>4</sub><sup>3−</sup>) are mutual competitors for the uptake by microalgal cells [<xref rid="B155-ijms-16-23929" ref-type="bibr">155</xref>]. A 10–fold increase in phosphate concentation resulted in a 18 times higher resistance of <italic>Monoraphidium arcuatum</italic> against As (V). On the other hand, a 10-fold decrease in medium nitrate NO<sub>3</sub><sup>−</sup> content at ordinary (PO<sub>4</sub><sup>3−</sup>) concentation, decreased by 28% <italic>Monoraphidium</italic> resistance towards arsenic [<xref rid="B65-ijms-16-23929" ref-type="bibr">65</xref>]. In another study, a 131-fold phosphate uplift improved 516 times resistance of <italic>Chlorella salina</italic> against As (V) [<xref rid="B35-ijms-16-23929" ref-type="bibr">35</xref>]. Indeed, increasing concentration of As (V) stimulated growth of arsene tolerant <italic>Chlorella</italic> sp. at low phosphate (P) concentration, although cell yields obtained were lower than in experiments with high P concentration [<xref rid="B36-ijms-16-23929" ref-type="bibr">36</xref>]. Concentration of PO<sub>4</sub><sup>3−</sup> in medium in relation to dissolved lead content can be also important, as Pb<sup>2+</sup> can precipitate in a form of Pb<sub>3</sub>(PO<sub>4</sub>)<sub>2</sub>, thereby removing available phosphate from solution and inhibiting growth of <italic>Chlamydomonas reinhardtii</italic> [<xref rid="B179-ijms-16-23929" ref-type="bibr">179</xref>].</p><p>Sulphur is a component of cysteine that participates in the defense mechanisms against heavy metals. The resistance of <italic>Chlamydomonas moewusii</italic> exposed to 4 mg/L cadmium can be improved five times and cysteine cell content can be raised 10 times, when sulphate (SO<sub>4</sub><sup>2−</sup>) concentration in medium is increased 100 times [<xref rid="B180-ijms-16-23929" ref-type="bibr">180</xref>]. In another study, a 10-fold increase in SO<sub>4</sub><sup>2−</sup> supply resulted in a <italic>Chlamydomonas reinhardtii</italic> resistance improved by up to 77% towards Cd. Improved <italic>Chlamydomonas</italic> resistance was accompanied with an increased activity of cysteine desulfhydrase, an enzyme responsible for the cleavage of cysteine into pyruvate, NH<sub>3</sub> and sulfide, the latter one reported to react with Cd to form CdS [<xref rid="B181-ijms-16-23929" ref-type="bibr">181</xref>].</p><p>A 20-fold increase in ammonium (NH<sub>4</sub><sup>+</sup>) concentration increased five times the accumulation of PO<sub>4</sub><sup>3−</sup> in <italic>Chlorella</italic><italic>vulgaris</italic> cells and caused a 50% alleviation in inhibition of <italic>Chlorella</italic> growth exerted by chromium (Cr) [<xref rid="B182-ijms-16-23929" ref-type="bibr">182</xref>]. Increase in magnesium (Mg<sup>2+</sup>) and hydrogen (H<sup>+</sup>) concentration reduced nickel toxicity towards <italic>Pseudokirchneriella subcapitata</italic>, as Mg<sup>2+</sup> and H<sup>+</sup> compete with Ni<sup>2+</sup> for the uptake by the cell transport system [<xref rid="B183-ijms-16-23929" ref-type="bibr">183</xref>]. In other studies, an increase in H<sup>+</sup> concentration was reported to improve, even up to 23 times [<xref rid="B184-ijms-16-23929" ref-type="bibr">184</xref>], <italic>Chlorella</italic> sp. resistance against Cu.</p><p>Zn alleviated detrimental effects of Cr on the photosynthetic mechanism in <italic>Micrasterias denticulata</italic> cells and Fe ameliorated inhibitory effect of Cd and Cr on <italic>Micrasterias</italic> cell development. Ca and Gd were reported to prevent alterations in cell morphology caused by Pb and Cd, thereby nullifying negative effects of Pb and Cd on <italic>Micrasterias</italic> cells [<xref rid="B185-ijms-16-23929" ref-type="bibr">185</xref>].</p><p>Finally, toxicity of thallium towards <italic>Chlorella</italic> sp. was completely alleviated, when concentration of K<sup>+</sup> in media was increased 20 times, presumably due to competive uptake in <italic>Chlorella</italic> cell transport systems [<xref rid="B71-ijms-16-23929" ref-type="bibr">71</xref>].</p><p>Cultivation parameters such as light intensity and CO<sub>2</sub> concentration are also important factors affecting microalgae response towards metals. Alterations in ligh irradiance had influence on inhibition or stimulation of <italic>Chlamydomonas reinhardtii</italic> growth under different Cu concentrations, and also affected accumulation of Cu in <italic>Chlamydomonas</italic> cells [<xref rid="B186-ijms-16-23929" ref-type="bibr">186</xref>]. Increase of CO<sub>2</sub> supply enabled the alleviation of the inhibitory effect of Cd towards <italic>Scenedesmus armatus</italic>, although growth inhibition was not entirely overcome [<xref rid="B140-ijms-16-23929" ref-type="bibr">140</xref>].</p></sec><sec id="sec4dot2-ijms-16-23929"><title>4.2. Supportive Compounds</title><p>Another modulating approach could be supplementation of microalgae cultures with organic compounds such as phytohormones or chelating agents.</p><sec id="sec4dot2dot1-ijms-16-23929"><title>4.2.1. Phytohormones: Modulating Effect</title><p>Phytohormones—spermidine (polyamine), gibberellin and many representatives of auxin and cytokinin groups—were reported to prevent inhibition of <italic>Chlorella vulgaris</italic> culture exposed to cadmium (Cd), copper (Cu) or lead (Pb) at a concentration of 0.1 mM. What is more, addition of compounds from the cytokinin group such as benzyladenine, zeatin, kinetin, 2-isopentenyladenine, diphenylurea, forchlorphenuron and thidiazuron not only enabled restoration of the <italic>Chlorella</italic> culture, but also increased cell number by up to 77%, when compared to control. Supplementation of spermidine, gibberellin, auxins or cytokinins generally increased not only the content of chlorophyll, carotenoid, protein, ascorbate and glutathione in <italic>Chlorella</italic> cells, but also activity of superoxide dismutase and catalase [<xref rid="B187-ijms-16-23929" ref-type="bibr">187</xref>]. In earlier studies, it was stated that the inhibitory effect of 0.1 mM Cd, Cu and Pb on <italic>Chlorella vulgaris</italic> culture can be also nullified in the presence of brassinolide [<xref rid="B154-ijms-16-23929" ref-type="bibr">154</xref>].</p></sec><sec id="sec4dot2dot2-ijms-16-23929"><title>4.2.2. Chelating Agents: Modulating Effect</title><p>Chelating agents are synthetized by microalgae for intracellular (phytochelatin, glutathione) or extracellular (exopolymers) detoxification of metals, but can also be added artificially into growth media to bind metals and modulate cell–metal interactions. Such agents can be low-molecular organic acids (ethylenediamine tetraacetic acid, nitrilotriacetic acid, citrate) or humic substances: humic acid or fulvic acid (<xref ref-type="table" rid="ijms-16-23929-t005">Table 5</xref>).</p><p>Addition of 34 µM ethylenediamine tetraacetic acid (EDTA) into <italic>Scenedesmus subspicatus</italic> culture enabled a ~55% reduction in growth inhibition exerted by ~40 µM Cu [<xref rid="B188-ijms-16-23929" ref-type="bibr">188</xref>]. Also EDTA, as well as nitrilotriacetic acid (NTA) and citrate (Cit), were reported to prevent accumulation of lanthanum (La), gadolinum (Gd) and yttrium (Y) in <italic>Chlorella vulgaris</italic> cells, with reduction in accumulation around 10- to 30-fold higher for EDTA, when compared to NTA and Cit [<xref rid="B189-ijms-16-23929" ref-type="bibr">189</xref>]. On the other hand, citrate was reported to enhance Cd (0.25 µM/L) accumulation and growth inhibition of <italic>Selenastrum capricornutum</italic>, due to the occasional uptake of Cd-citrate by cells [<xref rid="B190-ijms-16-23929" ref-type="bibr">190</xref>]. With the absence of EDTA in growth medium, cadmium (Cd) exerted much stronger inhibitory effects on <italic>Scenedesmus armatus</italic>, when compared to the growth in EDTA-containing medium [<xref rid="B69-ijms-16-23929" ref-type="bibr">69</xref>]. Growth of <italic>Scenedesmus quadricauda</italic> or <italic>Microcystis aeruginosa</italic> in the presence of lanthanum (0.72–72 µM) and EDTA (0.269–26.9 µM) was inhibited or enhanced, depending on La and EDTA concentrations. EDTA (2.69–13.4 µM) vastly alleviated the inhibitory effect of La on <italic>Microcystis</italic> growth, although EDTA alone and at higher concentration had strong inhibitory effects towards <italic>Microcystis</italic> [<xref rid="B42-ijms-16-23929" ref-type="bibr">42</xref>]. EDTA [<xref rid="B37-ijms-16-23929" ref-type="bibr">37</xref>,<xref rid="B191-ijms-16-23929" ref-type="bibr">191</xref>,<xref rid="B192-ijms-16-23929" ref-type="bibr">192</xref>] or citrate [<xref rid="B37-ijms-16-23929" ref-type="bibr">37</xref>,<xref rid="B193-ijms-16-23929" ref-type="bibr">193</xref>] increased Fe availability to microalgae, although high concentration of chelating agent can have opposite effects [<xref rid="B42-ijms-16-23929" ref-type="bibr">42</xref>,<xref rid="B191-ijms-16-23929" ref-type="bibr">191</xref>]. Additionally, EDTA that fails to maintain availabilily of Fe at high pH during <italic>Spirulina</italic> cultivation, can be replaced by alternative chelating agents such as Fe complexes of <italic>N</italic>,<italic>Nʹ</italic>-bis(2-hydroxybenzyl)ethylenediamine-<italic>N</italic>,<italic>N'</italic>-diacetic acid (HBED), ethylenediamine-<italic>N</italic>,<italic>N'</italic>-bis((2-hydroxyphenyl)acetic acid) (EDDHA) or ethylenediamine-<italic>N</italic>,<italic>N'</italic>-bis((2-hydroxy-4-methylphenyl)acetic acid) (EDDHMA) [<xref rid="B194-ijms-16-23929" ref-type="bibr">194</xref>].</p><p>Humic acid was reported to protect <italic>Dunaliella salina</italic> and <italic>Nannochloropsis salina</italic> cells against Ni<sup>2+</sup> stress, by means of forming humic acid–Ni<sup>2+</sup> complexes and/or by adsorbing on cell surface and thus, creating an additional barrier for Ni<sup>2+</sup> uptake [<xref rid="B118-ijms-16-23929" ref-type="bibr">118</xref>]. Similarly, humic acids reduced toxicity of Cd<sup>2+</sup> and Zn<sup>2+</sup> towards <italic>Pseudokirchneriella subcapitata</italic> [<xref rid="B195-ijms-16-23929" ref-type="bibr">195</xref>], Hg<sup>2+</sup> towards <italic>Isochrysis galbana</italic> [<xref rid="B196-ijms-16-23929" ref-type="bibr">196</xref>] and ZnO nanoparticles towards <italic>Anabaena</italic> sp [<xref rid="B197-ijms-16-23929" ref-type="bibr">197</xref>]. Humic acid itself at 7 and 2.5–10 mg/L stimulated growth of <italic>Isochrysis galbana</italic> [<xref rid="B198-ijms-16-23929" ref-type="bibr">198</xref>] and <italic>Stichococcus bacillaris</italic> [<xref rid="B141-ijms-16-23929" ref-type="bibr">141</xref>], presumably due to improved nutrient uptake via humic acid–cell membranes interaction [<xref rid="B198-ijms-16-23929" ref-type="bibr">198</xref>]. However, an opposite effect, enhanced toxicity of Pb towards <italic>Isochrysis</italic> in the presence humic acid, was also observed [<xref rid="B198-ijms-16-23929" ref-type="bibr">198</xref>], because the formation of a ternary complex between Pb, humic acid and microalga cell surface, enhances internalization of Pb [<xref rid="B199-ijms-16-23929" ref-type="bibr">199</xref>]. Humic acid was also reported to be inhibitory (0.3 mg/L) and lethal (1 mg/L) for <italic>Anabaena circinalis</italic>, probably due to its chelating activity towards Fe<sup>3+</sup>, leading to the decrease in availability of Fe necessary for <italic>Anabaena</italic> growth [<xref rid="B200-ijms-16-23929" ref-type="bibr">200</xref>]. It is also noteworthy, that humic acid can undergo degradation under high light irradiance, leading to the decreased capacity for metal complexation [<xref rid="B201-ijms-16-23929" ref-type="bibr">201</xref>]. Fulvic acid contributed to protection of <italic>Scenedesmus subspicatus</italic> against Cu<sup>2+</sup> [<xref rid="B188-ijms-16-23929" ref-type="bibr">188</xref>], but no protective effect against Cd<sup>2+</sup> and Zn<sup>2+</sup> was found for <italic>Pseudokirchneriella subcapitata</italic> [<xref rid="B195-ijms-16-23929" ref-type="bibr">195</xref>]. Fulvic acid was also reported to serve as a source of phosphorus to nullify toxic effects of aluminum (Al) on P-metabolism in <italic>Chlorella pyrenoidosa</italic> [<xref rid="B202-ijms-16-23929" ref-type="bibr">202</xref>].</p><table-wrap id="ijms-16-23929-t005" position="float"><object-id pub-id-type="pii">ijms-16-23929-t005_Table 5</object-id><label>Table 5</label><caption><p>Effect of humic and fulvic acids on microalgae response towards metals.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Chelating Agent</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Metal</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Uplift of Chelating Agent Concentration</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Strain</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reduction of Growth Inhibition</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Humic acid (Soil)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Ni<sup>2+</sup> (0.5 mg/L)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→0.2 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Dunaliella salina Nannochloropsis salina</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">40% <sup>A</sup>→25% <sup>C</sup>30% <sup>A</sup>→15% <sup>C</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B118-ijms-16-23929" ref-type="bibr">118</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Humic acid (Soil)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cd<sup>2+</sup> (0.2 mg/L)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→5 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Pseudokirchneriella subcapitata</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">52% <sup>A</sup>→28% <sup>C</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B195-ijms-16-23929" ref-type="bibr">195</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Humic acid (Soil)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Zn<sup>2+</sup> (0.39 mg/L)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→5 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Pseudokirchneriella subcapitata</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">55% <sup>A</sup>→4% <sup>C</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B195-ijms-16-23929" ref-type="bibr">195</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Humic acid (Peat)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cd<sup>2+</sup> (0.2 mg/L)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→5 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Pseudokirchneriella subcapitata</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">52% <sup>A</sup>→8% <sup>C</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B195-ijms-16-23929" ref-type="bibr">195</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Humic acid (Peat)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Zn<sup>2+</sup> (0.39 mg/L)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→5 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Pseudokirchneriella subcapitata</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">55% <sup>A</sup>→30% <sup>C</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B195-ijms-16-23929" ref-type="bibr">195</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Humic acid</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">As(III) (100 µM)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→10 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Stichococcus bacillaris</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">52% <sup>A</sup>→33% <sup>C</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B141-ijms-16-23929" ref-type="bibr">141</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Humic acid (Sediment)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Hg<sup>2+</sup> (10 ppb)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→10 ppm</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Isochrysis galbana</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Complete reduction in growth inhibition plus stimulation</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B196-ijms-16-23929" ref-type="bibr">196</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Humic acid</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">ZnO–NPs (1 mg/L)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→3 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Anabaena</italic> sp.</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">70% <sup>A</sup>→40% <sup>C</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B197-ijms-16-23929" ref-type="bibr">197</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Fulvic acid (Sediment)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cu<sup>2+</sup> (~5 µM)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">1→5 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Scenedesmus subspicatus</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">56% <sup>A1</sup>→30% <sup>C1</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B188-ijms-16-23929" ref-type="bibr">188</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Fulvic acid (Suwannee River)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cd<sup>2+</sup> (0.2 mg/L)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→5 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Pseudokirchneriella subcapitata</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">52% <sup>A</sup>→45% <sup>C</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B195-ijms-16-23929" ref-type="bibr">195</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Fulvic acid (Suwannee River)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Zn<sup>2+</sup> (0.39 mg/L)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→5 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Pseudokirchneriella subcapitata</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">No reduction in growth inhibition</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B195-ijms-16-23929" ref-type="bibr">195</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Fulvic acid (Soil)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Al <sup>i+o</sup> (6 µM)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→11 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Chlorella pyrenoidosa</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Complete reduction in growth inhibition plus stimulation</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B202-ijms-16-23929" ref-type="bibr">202</xref>]</td></tr></tbody></table><table-wrap-foot><fn><p><sup>A</sup> growth inhibition in the absence of chelating agent; <sup>A1</sup>, growth inhibition in the presence of decreased amount of chelating agent; <sup>C</sup> growth inhibition in the presence of chelating agent; <sup>C1</sup>, growth inhibition in the presence of increased amount of chelating agent; <sup>i+o</sup>, a sum of inorganic and organic aluminum.</p></fn></table-wrap-foot></table-wrap></sec><sec id="sec4dot2dot3-ijms-16-23929"><title>4.2.3. Nanoparticles: Modulating Effect</title><p>The presence of metallic and non-metallic nanomaterials can alter the effect of metals on microalgae. For instance, the presence of graphene oxide (GO) increased toxicity of Cd towards <italic>Microcystis aeruginosa</italic> [<xref rid="B203-ijms-16-23929" ref-type="bibr">203</xref>], while Cd toxicity towards <italic>Chlamydomonas reinhardtii</italic> was reduced in the presence of titanium dioxide engineered nanoparticles (ENPs) [<xref rid="B204-ijms-16-23929" ref-type="bibr">204</xref>]. TiO<sub>2</sub> nanoparticles and Zn ions in the mixture exerted the enhanced or decreased toxicity towards <italic>Anabaena</italic> sp., depending on mutual interactions between different concentrations of TiO<sub>2</sub> and Zn [<xref rid="B73-ijms-16-23929" ref-type="bibr">73</xref>]. Finally, the presence of engineered nanoparticles was reported to decrease intracellular content of Cu and Pb in <italic>Chlorella kesslerii</italic> and wall-possessing <italic>Chlamydomonas reinhardtii</italic>, as metal binding to nanoparticles reduces availability of Cu and Pb to these microalgal strains [<xref rid="B205-ijms-16-23929" ref-type="bibr">205</xref>].</p></sec><sec id="sec4dot2dot4-ijms-16-23929"><title>4.2.4. Macrocycles: Modulating Effect</title><p>Supramolecular water soluble compounds such as cyclodextrins, calixarenes and resorcinarenes can possibly change interactions between microalgae and metals.</p><p>Cyclodextrins (CDs) are macrocyclic oligosaccharides composed of six, seven, or eight (α 1–4) glucosidic units and called: α,β and γ-CDs, respectively. They are produced from enzymatic hydrolysis of starch, with cycloglycosyl transferase amylases (CGTases) [<xref rid="B206-ijms-16-23929" ref-type="bibr">206</xref>,<xref rid="B207-ijms-16-23929" ref-type="bibr">207</xref>]. CDs are ring molecules, either toroidal or cone shaped, but not cylindrical [<xref rid="B208-ijms-16-23929" ref-type="bibr">208</xref>]. The primary hydroxyl groups are situated on the narrow side while, the secondary groups are located on the wider side. The central cavity of CDs is hydrophobic, while the outer part is hydrophilic due the presence of hydroxyl groups [<xref rid="B209-ijms-16-23929" ref-type="bibr">209</xref>]. β-cyclodextrins can possess methyl, carboxymethyl or hydroxypropyl moieties [<xref rid="B210-ijms-16-23929" ref-type="bibr">210</xref>,<xref rid="B211-ijms-16-23929" ref-type="bibr">211</xref>] and form complexes with metals [<xref rid="B212-ijms-16-23929" ref-type="bibr">212</xref>], phytosterols [<xref rid="B213-ijms-16-23929" ref-type="bibr">213</xref>] and carotenoids [<xref rid="B214-ijms-16-23929" ref-type="bibr">214</xref>]. Carboxymethyl-β-cyclodextrin (3.3 mM) was successfully harnessed for reduction of metal (Cd, Co, Cu) toxicity towards naphthalene-degrading bacterium <italic>Burkholderia</italic> sp. [<xref rid="B215-ijms-16-23929" ref-type="bibr">215</xref>]. On the other hand, alhough hydroxypropyl-β-cyclodextrin up to 20 mM did not itself cause inhibition of microalga <italic>Selenastrum capricornutum</italic> growth, it failed to protect this microalga strain against Zn toxicity [<xref rid="B216-ijms-16-23929" ref-type="bibr">216</xref>], because hydroxypropyl-β-cyclodextrin does not possess metal-binding substituents [<xref rid="B215-ijms-16-23929" ref-type="bibr">215</xref>].</p><p>Calix[<italic>n</italic>]arenes and resorcin[4]arenes are macrocyclic compounds consisting of phenol or resorcinol units, respectively, which are cyclically linked by aliphatic bridges [<xref rid="B217-ijms-16-23929" ref-type="bibr">217</xref>]. Calix[<italic>n</italic>]arenes (<italic>n</italic> = 4, 5, 6, 7 and 8) are obtained as a result of condensation of <italic>p</italic>-<italic>tert</italic>-butylphenol with formaldehyde under alkaline catalysis [<xref rid="B218-ijms-16-23929" ref-type="bibr">218</xref>,<xref rid="B219-ijms-16-23929" ref-type="bibr">219</xref>,<xref rid="B220-ijms-16-23929" ref-type="bibr">220</xref>], whereas resorcin[4]arenes are formed as a result of acid-catalysed reaction between resorcinol and aliphatic or aromatic aldehydes [<xref rid="B221-ijms-16-23929" ref-type="bibr">221</xref>]. Water-soluble calix[4]arenes and resorcin[4]arenes possess charged groups (ammonium, sulphonium, carboxylate, phosphate) or hydrophilic fragments [<xref rid="B222-ijms-16-23929" ref-type="bibr">222</xref>,<xref rid="B223-ijms-16-23929" ref-type="bibr">223</xref>,<xref rid="B224-ijms-16-23929" ref-type="bibr">224</xref>,<xref rid="B225-ijms-16-23929" ref-type="bibr">225</xref>]. Derivatives of calix[<italic>n</italic>]arenes such as <italic>p</italic>-sulphonate or methoxycarboxylic derivatives form stable complexes with Zn<sup>2+</sup>, Cu<sup>2+</sup>, Ni<sup>2+</sup> under neutral or alkaline conditions [<xref rid="B226-ijms-16-23929" ref-type="bibr">226</xref>,<xref rid="B227-ijms-16-23929" ref-type="bibr">227</xref>,<xref rid="B228-ijms-16-23929" ref-type="bibr">228</xref>]. Water soluble resorcin[4]arene derivatives are able to form complexes, not only with the metal ions, but also with amino acids, sugars, and nucleosides [<xref rid="B229-ijms-16-23929" ref-type="bibr">229</xref>,<xref rid="B230-ijms-16-23929" ref-type="bibr">230</xref>,<xref rid="B231-ijms-16-23929" ref-type="bibr">231</xref>]. It was demonstrated that <italic>p</italic>-sulfonatocalix[4,6,8]arene and <italic>C</italic>-nonylresorcin[4]arene possess antimicrobial activity against fungal and bacterial microorganisms [<xref rid="B232-ijms-16-23929" ref-type="bibr">232</xref>]. Additionally, <italic>C</italic>-methylcalix[4]-resorcinarene containing pyridinium salt, was reported to exhibit a selective inhibitory effect on Gram-positive bacteria [<xref rid="B233-ijms-16-23929" ref-type="bibr">233</xref>].</p><p>Water soluble supramolecular molecules have the potential to modify interactions between metals and microorganisms such as microalgae, but their application in this field is highly unexplored.</p></sec></sec><sec id="sec4dot3-ijms-16-23929"><title>4.3. Development of Strain Tolerance to Metals</title><p>Some microalgae are able to inhabit environments contaminated by heavy metals. Such microalgal strains possess uplifted tolerance towards heavy metals [<xref rid="B104-ijms-16-23929" ref-type="bibr">104</xref>,<xref rid="B234-ijms-16-23929" ref-type="bibr">234</xref>,<xref rid="B235-ijms-16-23929" ref-type="bibr">235</xref>,<xref rid="B236-ijms-16-23929" ref-type="bibr">236</xref>,<xref rid="B237-ijms-16-23929" ref-type="bibr">237</xref>]. Increased tolerance can be also induced on laboratory scale by applying proper metal dosages [<xref rid="B238-ijms-16-23929" ref-type="bibr">238</xref>,<xref rid="B239-ijms-16-23929" ref-type="bibr">239</xref>] or metal-containing wastes [<xref rid="B240-ijms-16-23929" ref-type="bibr">240</xref>]. It results in development of physiologically adapted strains [<xref rid="B61-ijms-16-23929" ref-type="bibr">61</xref>,<xref rid="B239-ijms-16-23929" ref-type="bibr">239</xref>,<xref rid="B241-ijms-16-23929" ref-type="bibr">241</xref>] or metal resistant mutants due to rare spontaneous mutations that occur before metal treatment [<xref rid="B61-ijms-16-23929" ref-type="bibr">61</xref>,<xref rid="B238-ijms-16-23929" ref-type="bibr">238</xref>,<xref rid="B239-ijms-16-23929" ref-type="bibr">239</xref>]. Microalgae with improved tolerance can become promising microbes for cultivation in metal polluted growth media and for production of target compounds [<xref rid="B104-ijms-16-23929" ref-type="bibr">104</xref>]. However, it should be taken into consideration that increased tolerance can be strictly strain–metal specific [<xref rid="B235-ijms-16-23929" ref-type="bibr">235</xref>] and a lack of inducing metal in the cultivation medium can have a negative effect on growth of metal resistant mutants [<xref rid="B238-ijms-16-23929" ref-type="bibr">238</xref>].</p></sec></sec><sec id="sec5-ijms-16-23929"><title>5. Strategy for Microalgal Production in the Presence of Metals</title><p>It has been widely reported that microalgae cultures, due to their ability for metal accumulation, can be used for bioremediation of heavy metal contaminated water/wastewater streams [<xref rid="B80-ijms-16-23929" ref-type="bibr">80</xref>,<xref rid="B242-ijms-16-23929" ref-type="bibr">242</xref>,<xref rid="B243-ijms-16-23929" ref-type="bibr">243</xref>]. In this review, other aspects of microalgae exposure to metals, such as production of numerous industrially important compounds from metal-exposed microalgae (<xref ref-type="table" rid="ijms-16-23929-t006">Table 6</xref>) and stategies to alter microalga–metal interactions for industrial microalgae productions, are discussed. As a result of metal exposure, microalgae are able to synthesize a range of target compounds: pigments, lipids, peptides, exopolymers, phytohormones, arsenoorganics or nanomaterials, as a defense mechanism against metal stress. Although metals induce synthesis of compounds by microalgae cells, they may also have detrimental effects on cell number, growth rate, cell dry weight, thereby diminishing productivity of target compounds in a metal-trigger system. For instance, an elevated copper (Cu) concentration increased chlorophyll and carotenoid content in <italic>Dunaliella</italic> cells [<xref rid="B244-ijms-16-23929" ref-type="bibr">244</xref>] and stimulated release of polysaccharides from <italic>Cylindrotheca fusiformis</italic> [<xref rid="B245-ijms-16-23929" ref-type="bibr">245</xref>] and phenolics from <italic>Dunaliella tertiolecta</italic> [<xref rid="B246-ijms-16-23929" ref-type="bibr">246</xref>] cells, though at the expense of a reduced number of cells in the culture. In other studies, the content of chlorophyll, protein and lipids in <italic>Chlorella vulgaris</italic> [<xref rid="B247-ijms-16-23929" ref-type="bibr">247</xref>], proline and total amino acids in <italic>Chlorella pyrenoidosa</italic> [<xref rid="B63-ijms-16-23929" ref-type="bibr">63</xref>] and chlorophyll and carotenoid in <italic>Pseudokirchneriella subcapitata</italic> [<xref rid="B248-ijms-16-23929" ref-type="bibr">248</xref>] increased in the presence of cadmium (Cd), chromium (Cr) and copper (Cu) respectively, but the growth in these cultures was considerably suppressed [<xref rid="B63-ijms-16-23929" ref-type="bibr">63</xref>,<xref rid="B247-ijms-16-23929" ref-type="bibr">247</xref>,<xref rid="B248-ijms-16-23929" ref-type="bibr">248</xref>]. A possible strategy to overcome this problem could be cultivation of microalgae under non-stressed conditions in order to obtain higher cells densities, with subsequent addition of metals for inducing stress and synthesis of target products in microalgae cells [<xref rid="B10-ijms-16-23929" ref-type="bibr">10</xref>]. Metals at higher concentration are toxic to microalgae, but at lower concentration can be stimulatory for growth (<xref ref-type="table" rid="ijms-16-23929-t001">Table 1</xref>). Additionaly, it was concluded that growth media might contain nutrients (Ca, Mg) in amounts that are not sufficient for some microalgal strains to achieve desirable growth [<xref rid="B249-ijms-16-23929" ref-type="bibr">249</xref>] and therefore some metal-containing effluents could also serve as a nutrient replacement for Ca [<xref rid="B41-ijms-16-23929" ref-type="bibr">41</xref>], Fe [<xref rid="B37-ijms-16-23929" ref-type="bibr">37</xref>] or Zn [<xref rid="B44-ijms-16-23929" ref-type="bibr">44</xref>] deficiency in growth media. Microalgae cultivation systems require large amounts of water [<xref rid="B250-ijms-16-23929" ref-type="bibr">250</xref>] and production of target compounds with metal polluted industrial water streams, instead of exploiting clean water sources, could be an additional advantage. Growth of cyanobacteria <italic>Nostoc linckia</italic> and <italic>Nostoc rivularis</italic> was stimulated at low loadings of (Zn, Cd)-containing sewage waters, but suppressed at high sewage water loadings [<xref rid="B251-ijms-16-23929" ref-type="bibr">251</xref>]. Industrial wastes/wastewaters contain not only metals, but also numerous organic pollutants (pesticides, pharmaceuticals, personal care products <italic>etc.</italic>) [<xref rid="B252-ijms-16-23929" ref-type="bibr">252</xref>] that can be harmful for microalgae cultures. Furthermore, although metal uptake occurs in microalgal cultures, high dosage wastes can strongly decrease productivity of microalgal cultivation [<xref rid="B251-ijms-16-23929" ref-type="bibr">251</xref>,<xref rid="B253-ijms-16-23929" ref-type="bibr">253</xref>]. Therefore, precautions should be taken to control concentration of metals and/or organic toxicants, so that optimal microalgal growth and product biosynthesis could be obtained.</p><p>An integrated process for metal (Al, Fe, Mn, Ba, Ce, La) remediation and lipid production in cultures of marine microalgae (<italic>Nannochloropsis</italic>, <italic>Pavlova</italic>, <italic>Tetraselmis</italic>, <italic>Chaetoceros</italic>) has already been proposed [<xref rid="B254-ijms-16-23929" ref-type="bibr">254</xref>]. Recently, a combination of heavy metal (Zn, Mn, Cd, Cu) removal to increase up to 2.17-fold lipid production from <italic>Chlorella minutissima</italic> has been described [<xref rid="B115-ijms-16-23929" ref-type="bibr">115</xref>]. Further, it was concluded that small concentrations of metal mixtures (As, Cd, Co, Cr, Cu, Hg, Ni, Pb, Se, Zn) present in coal fired flue gas could increase lipid yield in <italic>Scenedesmus obliquus</italic> cultures by 61% [<xref rid="B255-ijms-16-23929" ref-type="bibr">255</xref>]. It was also suggested that uptake of lead (Pb) from textile dyeing industry effluent by <italic>Neochloris</italic> sp. could be accompanied with accumulation of cell neutral lipid content with increased levels of oleic (C18:1) acid [<xref rid="B256-ijms-16-23929" ref-type="bibr">256</xref>]. Additionally, metal exposure can lead to modifications in fatty acid profiles in microalgal cells, thereby improving quality of biodiesel [<xref rid="B117-ijms-16-23929" ref-type="bibr">117</xref>]. Finally, the uptake of metals (Cr, Mn, Fe, Co, Ni, Cu, Mo, Cd, Pb) from landfill leachate combined with hydrogen production in <italic>Chlamydomonas reinhardtii</italic> cultures, has been discussed [<xref rid="B257-ijms-16-23929" ref-type="bibr">257</xref>]. It should be noted that products, synthesized by microalgae cells in response to metal stress, can be contaminated by metals. The presence of metals in final products might not be appropriate in terms of application for food or medical purposes. Therefore, desorption methods (EDTA, diethyl dithiocarbamate, carbonate, dicarbonate) should be applied to obtain a metal free product, without causing the degradation of the product structure. Moreover, monitoring to maintain metal concentration in a final product below allowable thresholds must be considered.</p><p>Microalgae are capable of absorbing heavy metals under photoautotrophic [<xref rid="B12-ijms-16-23929" ref-type="bibr">12</xref>,<xref rid="B80-ijms-16-23929" ref-type="bibr">80</xref>,<xref rid="B242-ijms-16-23929" ref-type="bibr">242</xref>,<xref rid="B243-ijms-16-23929" ref-type="bibr">243</xref>] and heterotrophic conditions [<xref rid="B234-ijms-16-23929" ref-type="bibr">234</xref>], and hence biocompound production under metal stress possibly could be achieved in open ponds, photobioreactors, but also in fermentation tanks [<xref rid="B258-ijms-16-23929" ref-type="bibr">258</xref>]. Strictly controlled media compositions can modulate microalgal sensitivity towards heavy metals also during a chemostat-based continuous cultivation [<xref rid="B59-ijms-16-23929" ref-type="bibr">59</xref>]. Additionally, an amount of microalgae biomass in relation to metal concentration should be taken into consideration, as high biomass densities can alleviate detrimental effect of metal ions on microalgae cells in culture [<xref rid="B259-ijms-16-23929" ref-type="bibr">259</xref>,<xref rid="B260-ijms-16-23929" ref-type="bibr">260</xref>]. The use of older culture inocullum also improved resistance of <italic>Scenedesmus quadricauda</italic> against Ag nanoparticles [<xref rid="B239-ijms-16-23929" ref-type="bibr">239</xref>]. Synergistic effects of different heavy metal ions [<xref rid="B261-ijms-16-23929" ref-type="bibr">261</xref>] or metal ions with nanoparticles (see <xref ref-type="sec" rid="sec4dot2dot3-ijms-16-23929">Section 4.2.3</xref>) on microalgae cells, should be also taken into consideration. Additionally, although nanoparticles can be synthetized by microalgae cells (see <xref ref-type="sec" rid="sec3dot7-ijms-16-23929">Section 3.7</xref>), the presence of nanoparticles can have negative effects on microalgae (<xref ref-type="table" rid="ijms-16-23929-t001">Table 1</xref>).</p><p>Composition of growth media and cultivation parameters have significant influence on microalgae resistance towards metal induced stress (see Chapter 4). Moreover, a modification of cultivation media with the change of metal concentration and/or composition can enhance not only growth, but also biosynthesis of target compounds. For instance, an alteration in Fe, Mn, Mo concentration and addition of Ni, caused the increase in biomass and hydrocarbon productivity in <italic>Botryococcus braunii</italic> culture [<xref rid="B262-ijms-16-23929" ref-type="bibr">262</xref>]. Also supplementation of growth medium for <italic>Chlorella vulgaris</italic> with 12 µM chelated Fe<sup>3+</sup>, resulted in an increase in <italic>Chlorella</italic> cell number by 27% and lipid content by 625%, when compared to the culture without Fe<sup>3+</sup> added [<xref rid="B263-ijms-16-23929" ref-type="bibr">263</xref>]. In another study, a six-fold uplift in Fe<sup>3+</sup> concentration enabled an increase of 22% lipid productivity in <italic>Nannochloropsis oculata</italic> culture [<xref rid="B264-ijms-16-23929" ref-type="bibr">264</xref>]. <italic>Anabaena variabilis</italic>, cultivated in a new vanadium (VO<sub>3</sub><sup>−</sup>)-containing growth media, produced 550% more hydrogen, and VO<sub>3</sub><sup>−</sup> was suggested as a microelement responsible for amplification of H<sub>2</sub> synthesis [<xref rid="B265-ijms-16-23929" ref-type="bibr">265</xref>]. Addition of 20 µg/L VO<sub>3</sub><sup>−</sup> into growth medium increased dry weight by up to 34%, and cell chlorophyll content by up to 100% in heterotrophically cultivated <italic>Scenedesmus obliquus</italic> [<xref rid="B37-ijms-16-23929" ref-type="bibr">37</xref>]. Further, 20 µg/L VO<sub>3</sub><sup>−</sup> stimulated production of zeaxanthin, lutein and β-carotene in <italic>Chlorella fusca</italic> cultivated at standard Fe medium concentration or Fe deficient conditions, and the stimulatory effect of VO<sub>3</sub><sup>−</sup> was more pronounced at standard Fe concentration [<xref rid="B266-ijms-16-23929" ref-type="bibr">266</xref>]. Vanadium, added as 1.25 mM Na<sub>3</sub>VO<sub>4</sub> to <italic>Haematococcus lacustris</italic> culture, increased carotenoid synthesis in cells and carotenoid productivity in culture respectively by 120% and 25%, after a two-day exposure. However, in a prolonged cultivation time, caronenoid productivity decreased drastically if compared to control, presumably due to inhibitory activity of Na<sub>3</sub>VO<sub>4</sub> towards protein tyrosine phosphatase (PTPase) [<xref rid="B39-ijms-16-23929" ref-type="bibr">39</xref>].</p><p>Supplementation of organic compounds into microalgal culture can be an additional protection in order to diminish interactions of metals from wastes to a level that enables metal-trigger production of target compounds, together with sufficient microalgal growth rate, even in high metal-level environment. Organic compounds such as phytohormones or various chelating agents inducing resistance mechanisms inside cells or creating a resistance barrier outside cells, can serve as a defense for cultivation of microalgae in high dose-metal contaminated systems. Interestingly, phytohormones can not only protect microalgae against metal stress [<xref rid="B154-ijms-16-23929" ref-type="bibr">154</xref>,<xref rid="B187-ijms-16-23929" ref-type="bibr">187</xref>], but can also improve growth [<xref rid="B267-ijms-16-23929" ref-type="bibr">267</xref>] and increase the content of saturated [<xref rid="B268-ijms-16-23929" ref-type="bibr">268</xref>] or unsaturated [<xref rid="B267-ijms-16-23929" ref-type="bibr">267</xref>] fatty acids in microalgae cells. Therefore, a proper design of media composition (micro/macro-elements, phytohormones, chelating agents, macrocycles) and cultivation conditions (CO<sub>2</sub>, light, temperature, pH) seems to be necessary in order to avoid detrimental effects of heavy metal ions and to obtain sufficient growth and productivity of target compounds in metal-exposed microalgae cultures. Finally, microalgae strains isolated from heavy metal polluted areas or developed in the laboratory, are able to tolerate increased metal concentrations and can become promising candidates for cultivation under metal stress [<xref rid="B104-ijms-16-23929" ref-type="bibr">104</xref>,<xref rid="B235-ijms-16-23929" ref-type="bibr">235</xref>,<xref rid="B236-ijms-16-23929" ref-type="bibr">236</xref>,<xref rid="B240-ijms-16-23929" ref-type="bibr">240</xref>,<xref rid="B241-ijms-16-23929" ref-type="bibr">241</xref>]. Such strains are more resistant against detrimental effects of metal exposure and could also be suitable for cultivation and synthesis of target products in outdoor open systems, as metal-stress conditions can prevent contamination by competitive or predatory micro and higher organisms [<xref rid="B9-ijms-16-23929" ref-type="bibr">9</xref>,<xref rid="B269-ijms-16-23929" ref-type="bibr">269</xref>].</p><table-wrap id="ijms-16-23929-t006" position="float"><object-id pub-id-type="pii">ijms-16-23929-t006_Table 6</object-id><label>Table 6</label><caption><p>Some examples of metal effects on microalgae growth and bioproduct synthesis.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Microalgae Strain</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Bioproduct</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Metal/s</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Bioproduct Synthesis <italic><sup>Info</sup></italic></th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Growth</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Pigments</italic></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Chlamydomonas acidophilla</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">β-carotene</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cu<sup>2+</sup> 0.1 g/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">120% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">–</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B103-ijms-16-23929" ref-type="bibr">103</xref>]</td></tr><tr><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Coccomyxa onubensis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1">Fe<sup>2+</sup></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B104-ijms-16-23929" ref-type="bibr">104</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Lutein</td><td align="center" valign="middle" rowspan="1" colspan="1">0.5 mM</td><td align="center" valign="middle" rowspan="1" colspan="1">~33% increase</td><td align="center" valign="middle" rowspan="1" colspan="1">35% increase</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Zeaxanthin</td><td align="center" valign="middle" rowspan="1" colspan="1">0.5 mM</td><td align="center" valign="middle" rowspan="1" colspan="1">~93% increase</td><td align="center" valign="middle" rowspan="1" colspan="1">35% increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">β-carotene</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0.5 mM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~35% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">35% increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Dunaliella salina</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">β-carotene</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Fe<sup>2+</sup> 0→450 µM <sup>Ac</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">7-fold increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">4-fold decrease</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B105-ijms-16-23929" ref-type="bibr">105</xref>]</td></tr><tr><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Nostoc minutum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1">As(V)</td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B34-ijms-16-23929" ref-type="bibr">34</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Chlorophyll a</td><td align="center" valign="middle" rowspan="1" colspan="1">0→1000 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">75% increase</td><td align="center" valign="middle" rowspan="1" colspan="1">66% increase</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Carotenoids</td><td align="center" valign="middle" rowspan="1" colspan="1">0→1000 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">40% increase</td><td align="center" valign="middle" rowspan="1" colspan="1">66% increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Allophycocyanin</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→1000 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">24.7% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">66% increase</td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Anabaena doliolum</italic></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1">Ni<sup>2+</sup></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B92-ijms-16-23929" ref-type="bibr">92</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Chlorophyll a</td><td align="center" valign="middle" rowspan="1" colspan="1">0→10 µM</td><td align="center" valign="middle" rowspan="1" colspan="1">~47% increase</td><td align="center" valign="middle" rowspan="1" colspan="1">35% increase <sup>24h</sup></td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">C-phycocyanin</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→0.1 µM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">4.35-fold increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">9% decrease <sup>96h</sup></td></tr><tr><td rowspan="2" align="center" valign="middle" colspan="1"><italic>Dunaliella salina</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Carotenoids</td><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Cu<sup>2+</sup>1 µM→20 µM</td><td align="center" valign="middle" rowspan="1" colspan="1">131% increase</td><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">>50% decrease</td><td rowspan="4" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B244-ijms-16-23929" ref-type="bibr">244</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Chlorophyll</td><td align="center" valign="middle" rowspan="1" colspan="1">62% increase</td></tr><tr><td rowspan="2" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Dunaliella tertiolecta</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Carotenoids</td><td align="center" valign="middle" rowspan="1" colspan="1">133% increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Chlorophyll</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">152% increase</td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Pseudokirchneriella subcapitata</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Chlorophyll a</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Cu<sup>2+</sup>0.5→60 µg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">10.3-fold increase</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Decrease (20% in growth rate and 72% in biomass)</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B248-ijms-16-23929" ref-type="bibr">248</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Chlorophyll b</td><td align="center" valign="middle" rowspan="1" colspan="1">15.4-fold increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Carotenoids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">4.1-fold increase</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Scenedesmus obliquus</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Chlorophyll</td><td align="center" valign="middle" rowspan="1" colspan="1">VO<sub>3</sub><sup>−</sup> 0→20 µg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">100% increase</td><td align="center" valign="middle" rowspan="1" colspan="1">34% increase</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B37-ijms-16-23929" ref-type="bibr">37</xref>]</td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1"><italic>Chlorella fusca</italic></td><td align="center" valign="middle" style="border-top:solid thin" rowspan="1" colspan="1">Lutein</td><td rowspan="3" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">VO<sub>3</sub><sup>−</sup> 0→20 µg/L <sup>SFeC</sup></td><td align="center" valign="middle" style="border-top:solid thin" rowspan="1" colspan="1">18% increase</td><td rowspan="3" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">–</td><td rowspan="3" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">[<xref rid="B266-ijms-16-23929" ref-type="bibr">266</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">β-carotene</td><td align="center" valign="middle" rowspan="1" colspan="1">400% increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Zeaxanthin</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">130% increase</td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Chlorella fusca</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Lutein</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">VO<sub>3</sub><sup>−</sup> 0→20 µg/L <sup>FeDC</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">17% increase</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">–</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B266-ijms-16-23929" ref-type="bibr">266</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">β-carotene</td><td align="center" valign="middle" rowspan="1" colspan="1">200% increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Zeaxanthin</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">40% increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Haematococcus lacustris</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Carotenoids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VO<sub>4</sub><sup>3−</sup>0→1.25 mM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">125% increase <sup>2DE</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">45% decrease <sup>2DE</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B39-ijms-16-23929" ref-type="bibr">39</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Haematococcus lacustris</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Carotenoids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VO<sub>4</sub><sup>3−</sup> 0→1.25 mM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">No increase <sup>4DE</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">40% decrease <sup>4DE</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B39-ijms-16-23929" ref-type="bibr">39</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Lipids</italic></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Chlorella minutissima</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cd<sup>2+</sup> 0→0.4 mM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~94% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~12% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B115-ijms-16-23929" ref-type="bibr">115</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Euglena gracilis</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cr<sup>6+</sup> 0→1.3 µM <sup>40%,1</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">44% increase <sup>40%,1</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IC<sub>50</sub> for 3.2 µM <sup>1</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B116-ijms-16-23929" ref-type="bibr">116</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Euglena gracilis</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cr<sup>6+</sup> 0→9.84 µM <sup>40%,2</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">28.5% increase <sup>40%,2</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IC<sub>50</sub> for 24.6 µM <sup>2</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B116-ijms-16-23929" ref-type="bibr">116</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Euglena gracilis</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cr<sup>6+</sup> 0→36.16 µM <sup>40%,3</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">100% increase <sup>40%,3</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IC<sub>50</sub> for 90.4 µM <sup>3</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B116-ijms-16-23929" ref-type="bibr">116</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Euglena gracilis</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cr<sup>6+</sup> 0→48.2 µM <sup>40%,4</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">10% increase <sup>40%,4</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">IC<sub>50</sub> for 120.5 µM <sup>4</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B116-ijms-16-23929" ref-type="bibr">116</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">TiO<sub>2</sub>-NPs 0→0.1 g/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">10% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">No change</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B74-ijms-16-23929" ref-type="bibr">74</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Arthrospira maxima</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nZVI-Nanofer 25 0→5.1 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">21% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">15% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B57-ijms-16-23929" ref-type="bibr">57</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Desmodesmus subspicatus</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nZVI-Nanofer 25 0→5.1 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">58% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">73% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B57-ijms-16-23929" ref-type="bibr">57</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Parachlorella kessleri</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nZVI-Nanofer 25 0→5.1 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">17% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">41% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B57-ijms-16-23929" ref-type="bibr">57</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Nannochloropsis limnetica</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Eicosapentaenoic acid C20:5</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nZVI-Nanofer 25 0→5.1 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">58 % increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">19% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B57-ijms-16-23929" ref-type="bibr">57</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Trachydiscus minutus</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Eicosapentaenoic acid C20:5</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">nZVI-Nanofer 25 0→5.1 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">34% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">31% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B57-ijms-16-23929" ref-type="bibr">57</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Scenedesmus obliquus</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">(As, Cd, Co, Cr, Cu, Hg, Ni, Pb, Se, Zn) as a mixture</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">61% increase <sup>1x</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">12% increase <sup>1x</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B255-ijms-16-23929" ref-type="bibr">255</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Neochloris sp.</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Oleic acid C18:1</td><td align="center" valign="middle" rowspan="1" colspan="1">Effluent from textile dyeing industry containing Pb <sup>Ut</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">Neutral lipid accumulation Oleic acid accumulation</td><td align="center" valign="middle" rowspan="1" colspan="1">–</td><td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B256-ijms-16-23929" ref-type="bibr">256</xref>]</td></tr><tr><td align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Fe<sup>3+</sup>/EDTA0→12 µM</td><td align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">7.25-fold increase</td><td align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">~27% increase</td><td align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B263-ijms-16-23929" ref-type="bibr">263</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Nannochloropsis oculata</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Fe<sup>3+</sup><sup>+EDTA</sup> 3.16→18.96 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">22% increase in production</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">–</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B264-ijms-16-23929" ref-type="bibr">264</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Exopolymers</italic></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Lyngbya putealis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1">Cu</td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">13% decrease</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B131-ijms-16-23929" ref-type="bibr">131</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Exopolysaccharides</td><td align="center" valign="middle" rowspan="1" colspan="1">0→2 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">2.43-fold increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Exoproteins</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→2 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">3.65-fold increase</td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Lyngbya putealis</italic></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1">Co</td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">21% decrease</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B131-ijms-16-23929" ref-type="bibr">131</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Exopolysaccharides</td><td align="center" valign="middle" rowspan="1" colspan="1">0→2 mg/L</td><td align="center" valign="middle" rowspan="1" colspan="1">2.09-fold increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Exoproteins</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→2 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2.64-fold increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Thalassiosira weissflogii</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Polysaccharides <sup>EPF</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Ag <sup>RENP</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~3.5-fold increase <sup>NL</sup> if: Ag 0.03→0.11 nM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">50% decrease <sup>NL</sup> if: Ag 0.01 nM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B132-ijms-16-23929" ref-type="bibr">132</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Thalassiosira weissflogii</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Polysaccharides <sup>EPF</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Ag <sup>RENP</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~6-fold increase <sup>NE</sup> if: Ag0.01→6.14 pM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">50% decrease <sup>NE</sup> if: Ag 2.16 pM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B132-ijms-16-23929" ref-type="bibr">132</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Thalassiosira pseudonana</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Proteins <sup>EPF</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cd <sup>RENP</sup> 0→0.05 nM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">50% increase <sup>CM,</sup><sup>NE</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">No change <sup>NE</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B133-ijms-16-23929" ref-type="bibr">133</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Thalassiosira pseudonana</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Carbohydrates <sup>EPF</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cd <sup>RENP</sup> 0→0.05 nM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2-fold increase <sup>CM,</sup><sup>NE</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">No change <sup>NE</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B133-ijms-16-23929" ref-type="bibr">133</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Cylindrotheca fusiformis</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Exopolysaccharides</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cu<sup>2+</sup> 0→0.5 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">100% increase <sup>RC</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">57% decrease</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B245-ijms-16-23929" ref-type="bibr">245</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Phytohormones</italic></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Chlorella vulgaris</italic></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Indole-acetic acid</td><td align="center" valign="middle" rowspan="1" colspan="1">Cd</td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B154-ijms-16-23929" ref-type="bibr">154</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">0→10<sup>−4</sup> M</td><td align="center" valign="middle" rowspan="1" colspan="1">~147% increase <sup>Ct</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">~35% decrease <sup>Ct</sup></td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→10<sup>−4</sup> M <sup>+B</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">3.6-fold increase <sup>Ct</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~8% decrease <sup>Ct</sup></td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Chlorella vulgaris</italic></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Zeatin</td><td align="center" valign="middle" rowspan="1" colspan="1">Pb</td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B154-ijms-16-23929" ref-type="bibr">154</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">0→10<sup>−4</sup> M</td><td align="center" valign="middle" rowspan="1" colspan="1">~35% increase <sup>Ct</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">~40% decrease <sup>Ct</sup></td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→10<sup>−4</sup> M <sup>+B</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~85% increase <sup>Ct</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~16% decrease <sup>Ct</sup></td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Chlorella vulgaris</italic></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Abscisic acid</td><td align="center" valign="middle" rowspan="1" colspan="1">Cu</td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B154-ijms-16-23929" ref-type="bibr">154</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">0→10<sup>−4</sup> M</td><td align="center" valign="middle" rowspan="1" colspan="1">~45% increase<sup>Ct</sup></td><td align="center" valign="middle" rowspan="1" colspan="1">~45% decrease <sup>Ct</sup></td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0→10<sup>−4</sup> M <sup>+B</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~65% increase<sup>Ct</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~24% decrease <sup>Ct</sup></td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Hydrogen</italic></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Chlamydomonas reinhardtii</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">H<sub>2</sub></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">16% leachate medium containing: (Cr, Mn, Fe, Co, Ni, Cu, Mo, Cd, Pb)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~37% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~50% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B257-ijms-16-23929" ref-type="bibr">257</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Anabaena variabilis</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">H<sub>2</sub></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">VO<sub>3</sub><sup>−</sup> 0→0.023 mg/L <sup>M</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">5.5-fold increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Delayed <sup>FSC</sup> No change in growth <sup>PCT</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B265-ijms-16-23929" ref-type="bibr">265</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"><italic>Other products</italic></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td><td align="center" valign="middle" rowspan="1" colspan="1"></td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Dunaliella tertiolecta</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Phenolics</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cu<sup>2+</sup> 0→0.79 µM</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">40% increase <sup>RC</sup></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">34% decrease</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B246-ijms-16-23929" ref-type="bibr">246</xref>]</td></tr><tr><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1"><italic>Chlorella vulgaris</italic></td><td align="center" valign="middle" rowspan="1" colspan="1">Chlorophyll a</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">Cd<sup>2+</sup> 0→0.1 µmol/L</td><td align="center" valign="middle" rowspan="1" colspan="1">~4–fold increase</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">~65% decrease</td><td rowspan="3" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">[<xref rid="B247-ijms-16-23929" ref-type="bibr">247</xref>]</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Protein</td><td align="center" valign="middle" rowspan="1" colspan="1">~5–fold increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">~3–fold increase</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Chlorella pyrenoidosa</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Proline Total Amino Acids</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cr<sup>6+</sup> 0→5 mg/L</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">240% increase 66% increase</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">60% decrease</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B63-ijms-16-23929" ref-type="bibr">63</xref>]</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Botryococcus braunii</italic></td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Hydrocarbons</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Modifications of culture media composition</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">27% increase after: Fe and Mn uplift + Mo decrease + Ni addition (1.73 µM)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">34% increase after: Fe and Mn decrease + Mo uplift + Ni addition (3.38 µM)</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B262-ijms-16-23929" ref-type="bibr">262</xref>]</td></tr></tbody></table><table-wrap-foot><fn><p><italic><sup>Info</sup></italic>, product synthesis expressed on various basis (cell content, dry weight, release from cells, concentration in the culture, productivity); <sup>Ac</sup>, with 67.5 mM acetate; <sup>24h</sup>, a 24h cultivation time; <sup>96h</sup>, a 96h cultivation time; <sup>SFeC</sup>, standard Fe concentration; <sup>FeDC</sup>, Fe deficient conditions; <sup>2DE</sup>, increase in cells after a 2-day exposure and compared to control cells at the same cultivation time; <sup>4DE</sup>, increase in cells after a 4-day exposure and compared to control cells at the same cultivation time; <sup>40%</sup>, concentration that constitutes 40% of a concentration necessary to obtain IC<sub>50</sub>; <sup>1</sup>, a UTEX strain cultivated in Buetow medium; <sup>2</sup>, a MAT strain cultivated in Buetow medium; <sup>3</sup>, a UTEX strain cultivated in C&M medium; <sup>4</sup>, a MAT strain cultivated in C&M medium; <sup>1x</sup>, for a lowest metal mixture tested; <sup>Ut</sup>, Pb was partially utilized by strain; <sup>+EDTA</sup>, a six fold increase in EDTA concentration also suggested; <sup>EPF</sup>, from Extracellular Polymeric Fraction; <sup>RENP</sup>, released from Engineered Nanoparticles; <sup>NL</sup>, nitrogen limited medium; <sup>NE</sup>, nutrient enriched medium; <sup>CM</sup>, in cultivation media; <sup>RC</sup>, the release from cells; <sup>+B</sup>, plus brassinolide 10<sup>−8</sup> M; <sup>Ct</sup>, when compared to control without heavy metal and brassinolide; <sup>M</sup>, composition and concentration of other micro/macro nutrients also changed; <sup>FSC</sup>, during the first stage of cultivation; <sup>PCT</sup>, in prolonged cultivation time.</p></fn></table-wrap-foot></table-wrap></sec><sec id="sec6-ijms-16-23929"><title>6. Summary</title><p>Metal exposure can be an interesting method to induce, in microalgae cells, the synthesis of target products such as pigments, lipids, peptides, exopolymers, phytohormones, arsenoorganics and nanoparticles. However, stimulation of target compound production in microalgae depends on many factors such as metal type and concentration or metal combination leading to synergistic effects, specificity of strain and cultivation parameters, and growth media composition, which all taken together determines the outcome of microalga response towards metal stress. Moreover, microalgae cultivation under stress conditions can stimulate production of target compounds, but usually at the expense of decreased growth rates, that diminishes overall productivity of metal exposed microalgae systems. The exception are resistant strains isolated from metal contaminated environments. A combination of metal removal from contaminated wastewaters, with metal-induced product biosynthesis, can be applied. Moreover, metal-containing wastewaters could also serve as a replenishment for microalgae growth in nutrient-deficient media. Suitable dosages of metals in relation to selected microalgae strain and adjusted growth conditions is key to develop efficient metal-exposed microalgal production systems.</p></sec></body><back><ack><title>Acknowledgments</title><p>This work was financed by AgricultureIsLife Platform at University of Liege-Gembloux Agro-Bio Tech.</p></ack><notes><title>Author Contributions</title><p>Krystian Miazek conducted literature research and wrote manuscript. Waldemar Iwanek wrote a part of manuscript concerning macrocycles. Claire Remacle provided expertise concerning metal uptake, oxidative stress and enzymatic reactions. Aurore Richel provided expertise in organometallic chemistry. Dorothee Goffin provided expertise in industrial applications of various products from microalgae. Additionally, Claire Remacle, Aurore Richel and Dorothee Goffin provided valuable comments, suggestions and corrections during the whole process of manuscript preparation.</p></notes><notes><title>Conflicts of Interest</title><p>The authors declare no conflict of interest.</p></notes><ref-list><title>References</title><ref id="B1-ijms-16-23929"><label>1.</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Leliaert</surname><given-names>F.</given-names></name><name><surname>Smith</surname><given-names>D.R.</given-names></name><name><surname>Moreau</surname><given-names>H.</given-names></name><name><surname>Herron</surname><given-names>M.D.</given-names></name><name><surname>Verbruggen</surname><given-names>H.</given-names></name><name><surname>Delwiche</surname><given-names>C.F.</given-names></name><name><surname>de Clerck</surname><given-names>O.</given-names></name></person-group><article-title>Phylogeny and molecular evolution of the green algae</article-title><source>CRC Crit. 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