Natural Products from Cyanobacteria: Focus on Beneficial Activities
Identifieur interne : 000664 ( Ncbi/Merge ); précédent : 000663; suivant : 000665Natural Products from Cyanobacteria: Focus on Beneficial Activities
Auteurs : Justine Demay ; Cécile Bernard ; Anita Reinhardt ; Benjamin MarieSource :
- Marine Drugs [ 1660-3397 ] ; 2019.
Abstract
Cyanobacteria are photosynthetic microorganisms that colonize diverse environments worldwide, ranging from ocean to freshwaters, soils, and extreme environments. Their adaptation capacities and the diversity of natural products that they synthesize, support cyanobacterial success in colonization of their respective ecological niches. Although cyanobacteria are well-known for their toxin production and their relative deleterious consequences, they also produce a large variety of molecules that exhibit beneficial properties with high potential in various fields (e.g., a synthetic analog of dolastatin 10 is used against Hodgkin’s lymphoma). The present review focuses on the beneficial activities of cyanobacterial molecules described so far. Based on an analysis of 670 papers, it appears that more than 90 genera of cyanobacteria have been observed to produce compounds with potentially beneficial activities in which most of them belong to the orders Oscillatoriales, Nostocales, Chroococcales, and Synechococcales. The rest of the cyanobacterial orders (i.e., Pleurocapsales, Chroococcidiopsales, and Gloeobacterales) remain poorly explored in terms of their molecular diversity and relative bioactivity. The diverse cyanobacterial metabolites possessing beneficial bioactivities belong to 10 different chemical classes (alkaloids, depsipeptides, lipopeptides, macrolides/lactones, peptides, terpenes, polysaccharides, lipids, polyketides, and others) that exhibit 14 major kinds of bioactivity. However, no direct relationship between the chemical class and the respective bioactivity of these molecules has been demonstrated. We further selected and specifically described 47 molecule families according to their respective bioactivities and their potential uses in pharmacology, cosmetology, agriculture, or other specific fields of interest. With this up-to-date review, we attempt to present new perspectives for the rational discovery of novel cyanobacterial metabolites with beneficial bioactivity.
Url:
DOI: 10.3390/md17060320
PubMed: 31151260
PubMed Central: 6627551
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PMC:6627551Le document en format XML
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<front><div type="abstract" xml:lang="en"><p>Cyanobacteria are photosynthetic microorganisms that colonize diverse environments worldwide, ranging from ocean to freshwaters, soils, and extreme environments. Their adaptation capacities and the diversity of natural products that they synthesize, support cyanobacterial success in colonization of their respective ecological niches. Although cyanobacteria are well-known for their toxin production and their relative deleterious consequences, they also produce a large variety of molecules that exhibit beneficial properties with high potential in various fields (e.g., a synthetic analog of dolastatin 10 is used against Hodgkin’s lymphoma). The present review focuses on the beneficial activities of cyanobacterial molecules described so far. Based on an analysis of 670 papers, it appears that more than 90 genera of cyanobacteria have been observed to produce compounds with potentially beneficial activities in which most of them belong to the orders Oscillatoriales, Nostocales, Chroococcales, and Synechococcales. The rest of the cyanobacterial orders (i.e., Pleurocapsales, Chroococcidiopsales, and Gloeobacterales) remain poorly explored in terms of their molecular diversity and relative bioactivity. The diverse cyanobacterial metabolites possessing beneficial bioactivities belong to 10 different chemical classes (alkaloids, depsipeptides, lipopeptides, macrolides/lactones, peptides, terpenes, polysaccharides, lipids, polyketides, and others) that exhibit 14 major kinds of bioactivity. However, no direct relationship between the chemical class and the respective bioactivity of these molecules has been demonstrated. We further selected and specifically described 47 molecule families according to their respective bioactivities and their potential uses in pharmacology, cosmetology, agriculture, or other specific fields of interest. With this up-to-date review, we attempt to present new perspectives for the rational discovery of novel cyanobacterial metabolites with beneficial bioactivity.</p>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Mar Drugs</journal-id>
<journal-id journal-id-type="iso-abbrev">Mar Drugs</journal-id>
<journal-id journal-id-type="publisher-id">marinedrugs</journal-id>
<journal-title-group><journal-title>Marine Drugs</journal-title>
</journal-title-group>
<issn pub-type="epub">1660-3397</issn>
<publisher><publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31151260</article-id>
<article-id pub-id-type="pmc">6627551</article-id>
<article-id pub-id-type="doi">10.3390/md17060320</article-id>
<article-id pub-id-type="publisher-id">marinedrugs-17-00320</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Natural Products from Cyanobacteria: Focus on Beneficial Activities</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-8044-8443</contrib-id>
<name><surname>Demay</surname>
<given-names>Justine</given-names>
</name>
<xref ref-type="aff" rid="af1-marinedrugs-17-00320">1</xref>
<xref ref-type="aff" rid="af2-marinedrugs-17-00320">2</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-7032-3989</contrib-id>
<name><surname>Bernard</surname>
<given-names>Cécile</given-names>
</name>
<xref ref-type="aff" rid="af1-marinedrugs-17-00320">1</xref>
<xref rid="c1-marinedrugs-17-00320" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Reinhardt</surname>
<given-names>Anita</given-names>
</name>
<xref ref-type="aff" rid="af2-marinedrugs-17-00320">2</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-9880-5541</contrib-id>
<name><surname>Marie</surname>
<given-names>Benjamin</given-names>
</name>
<xref ref-type="aff" rid="af1-marinedrugs-17-00320">1</xref>
</contrib>
</contrib-group>
<aff id="af1-marinedrugs-17-00320"><label>1</label>
UMR 7245 MCAM, Muséum National d’Histoire Naturelle-CNRS, Paris, 12 rue Buffon, CP 39, 75231 Paris CEDEX 05, France;<email>justine.demay1@mnhn.fr</email>
(J.D.);<email>benjamin.marie@mnhn.fr</email>
(B.M.)</aff>
<aff id="af2-marinedrugs-17-00320"><label>2</label>
Thermes de Balaruc-les-Bains, 1 rue du Mont Saint-Clair BP 45, 34540 Balaruc-Les-Bains, France;<email>anita.reinhardt@thermesbalaruc.com</email>
</aff>
<author-notes><corresp id="c1-marinedrugs-17-00320"><label>*</label>
Correspondence: <email>cecile.bernard@mnhn.fr</email>
; Tel.: +33-1-40-79-31-83/95</corresp>
</author-notes>
<pub-date pub-type="epub"><day>30</day>
<month>5</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="collection"><month>6</month>
<year>2019</year>
</pub-date>
<volume>17</volume>
<issue>6</issue>
<elocation-id>320</elocation-id>
<history><date date-type="received"><day>15</day>
<month>4</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>21</day>
<month>5</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© 2019 by the authors.</copyright-statement>
<copyright-year>2019</copyright-year>
<license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) 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>Cyanobacteria are photosynthetic microorganisms that colonize diverse environments worldwide, ranging from ocean to freshwaters, soils, and extreme environments. Their adaptation capacities and the diversity of natural products that they synthesize, support cyanobacterial success in colonization of their respective ecological niches. Although cyanobacteria are well-known for their toxin production and their relative deleterious consequences, they also produce a large variety of molecules that exhibit beneficial properties with high potential in various fields (e.g., a synthetic analog of dolastatin 10 is used against Hodgkin’s lymphoma). The present review focuses on the beneficial activities of cyanobacterial molecules described so far. Based on an analysis of 670 papers, it appears that more than 90 genera of cyanobacteria have been observed to produce compounds with potentially beneficial activities in which most of them belong to the orders Oscillatoriales, Nostocales, Chroococcales, and Synechococcales. The rest of the cyanobacterial orders (i.e., Pleurocapsales, Chroococcidiopsales, and Gloeobacterales) remain poorly explored in terms of their molecular diversity and relative bioactivity. The diverse cyanobacterial metabolites possessing beneficial bioactivities belong to 10 different chemical classes (alkaloids, depsipeptides, lipopeptides, macrolides/lactones, peptides, terpenes, polysaccharides, lipids, polyketides, and others) that exhibit 14 major kinds of bioactivity. However, no direct relationship between the chemical class and the respective bioactivity of these molecules has been demonstrated. We further selected and specifically described 47 molecule families according to their respective bioactivities and their potential uses in pharmacology, cosmetology, agriculture, or other specific fields of interest. With this up-to-date review, we attempt to present new perspectives for the rational discovery of novel cyanobacterial metabolites with beneficial bioactivity.</p>
</abstract>
<kwd-group><kwd>cyanobacteria</kwd>
<kwd>natural products</kwd>
<kwd>metabolites</kwd>
<kwd>biological activities</kwd>
<kwd>producers</kwd>
<kwd>chemical classes</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="marinedrugs-17-00320-f001" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Evolution of the cumulative number of metabolite families according to the number of analyzed publications used for the construction of the database. The arrow indicates a reclassification event of all the structural variants of one molecule in a unique entry of “family” [<xref rid="B13-marinedrugs-17-00320" ref-type="bibr">13</xref>
,<xref rid="B25-marinedrugs-17-00320" ref-type="bibr">25</xref>
,<xref rid="B26-marinedrugs-17-00320" ref-type="bibr">26</xref>
]. We observed a progressive stabilization of the number of compound families in the database that supports the postulation of the exhaustiveness of the present database.</p>
</caption>
<graphic xlink:href="marinedrugs-17-00320-g001"></graphic>
</fig>
<fig id="marinedrugs-17-00320-f002" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>Proportion of families of compound by taxonomical level. (<bold>A</bold>
) The pie chart represents the percentage of compound families for each taxonomical family. Note that some compound families can be produced by several cyanobacterial families. The “Other” category concerns other taxonomical families that produce less than two compound families. (<bold>B</bold>
) The histogram shows the number of compound families for each genus. The “Other” category corresponds to genera producing less than four compound families. * indicates cyanobacterial assemblages whom the real metabolite producer is still undetermined. The boxes indicate the environmental origins for the corresponding genera. For both charts, the colors correspond to the taxonomical order of each genus or family.</p>
</caption>
<graphic xlink:href="marinedrugs-17-00320-g002"></graphic>
</fig>
<fig id="marinedrugs-17-00320-f003" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>Classification of the 260 cyanobacterial metabolite families according to their respective chemical classes. All the molecules have been classified into these different classes according to their respective structural characteristics. For example, the depsipeptides are a class of peptides containing an ester bond and macrolides are molecules exhibiting a macrocycle and one or more lactone functions. Some examples of cyanobacterial molecules belonging to these classes are illustrated. Hapalindole A (alkaloids), Oscillapeptin A (depsipeptides), Minutissamide A (lipopeptides), Caylobolide B (macrolides/lactones), Anabaenopeptin E (peptides), β-carotene (terpenes), Cyclodextrin phosphate (polysaccharides), Lyngbic acid (lipids), and Cylindrocyclophane A (polyketides). The main characteristics of each chemical class are highlighted in red. All the structures were obtained from the ChEMBL Database (<uri xlink:href="https://www.ebi.ac.uk/chembl/">https://www.ebi.ac.uk/chembl/</uri>
).</p>
</caption>
<graphic xlink:href="marinedrugs-17-00320-g003"></graphic>
</fig>
<fig id="marinedrugs-17-00320-f004" orientation="portrait" position="float"><label>Figure 4</label>
<caption><p>Number of metabolite families observed for each type of activity. The percentage represents the proportion of one activity compared to the whole occurrence of activities detected (n = 362). Some compounds present various activities and are considered several times.</p>
</caption>
<graphic xlink:href="marinedrugs-17-00320-g004"></graphic>
</fig>
<fig id="marinedrugs-17-00320-f005" orientation="portrait" position="float"><label>Figure 5</label>
<caption><p>Classification of the 260 metabolite families according to their respective activities and chemical classes. The number of metabolite families is symbolized by the disc diameters, for each activity and each chemical class. For example, the first circle represents the number of alkaloids that exhibit a hepatotoxic activity (in this case, one family of metabolites). Colors correspond to the different categories of activity targets. For example, cytotoxicity and hepatotoxicity are tested in vitro against cell lines while neurotoxicity, antioxidant, and anti-inflammatory activities can be biochemically tested for specific cellular mechanisms (such as the sodium influx, the scavenging of ROS (reactive oxygen species), and the inhibition of cytokines).</p>
</caption>
<graphic xlink:href="marinedrugs-17-00320-g005"></graphic>
</fig>
<table-wrap id="marinedrugs-17-00320-t006" orientation="portrait" position="float"><object-id pub-id-type="pii">marinedrugs-17-00320-t006_Table 6</object-id>
<label>Table 6</label>
<caption><p>Cytotoxic metabolites extracted from the database.</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">Molecule Family</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Chemical Classes</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Activity</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Producing Organisms</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Tubercidin</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Nucleoside</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Cytotoxic<break></break>
-Microtubule stabilizer</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Tolypothrix byssoidea</italic>
H-6-2,<break></break>
<italic>Scytonema saleyeriense</italic>
var. <italic>indica</italic>
CV-14-1,<break></break>
<italic>Plectonema radiosum</italic>
DF-6-1,<break></break>
<italic>Tolypothrix distorta</italic>
BL-11-2</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B198-marinedrugs-17-00320" ref-type="bibr">198</xref>
,<xref rid="B199-marinedrugs-17-00320" ref-type="bibr">199</xref>
,<xref rid="B200-marinedrugs-17-00320" ref-type="bibr">200</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Aurilides</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Depsipeptide</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Cytotoxic<break></break>
-Lethal activity<break></break>
-Anti-swarming<break></break>
-Antiprotozoal<break></break>
-Induce loss of microfilament network</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Lyngbya majuscula</italic>
,<break></break>
<italic>Okeania</italic>
sp.,<break></break>
<italic>Lyngbya</italic>
sp.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B70-marinedrugs-17-00320" ref-type="bibr">70</xref>
,<xref rid="B202-marinedrugs-17-00320" ref-type="bibr">202</xref>
,<xref rid="B203-marinedrugs-17-00320" ref-type="bibr">203</xref>
,<xref rid="B204-marinedrugs-17-00320" ref-type="bibr">204</xref>
,<xref rid="B205-marinedrugs-17-00320" ref-type="bibr">205</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Swinholide-type</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Macrolide</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Cytotoxic<break></break>
-Actin microfilament disruption</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Symploca</italic>
sp.,<break></break>
<italic>Geitlerinema</italic>
sp.,<break></break>
<italic>Nostoc</italic>
sp. UHCC0451,<break></break>
<italic>Phormidium</italic>
sp.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B206-marinedrugs-17-00320" ref-type="bibr">206</xref>
,<xref rid="B207-marinedrugs-17-00320" ref-type="bibr">207</xref>
,<xref rid="B208-marinedrugs-17-00320" ref-type="bibr">208</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Anabaenolysins</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Lipopeptide</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Cytotoxic<break></break>
-Antifungal<break></break>
-Hemolytic activity<break></break>
-Ability to permeabilize cell membranes</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Anabaena</italic>
sp. XPORK 15F,<break></break>
<italic>Anabaena</italic>
sp. XSPORK 27C</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B209-marinedrugs-17-00320" ref-type="bibr">209</xref>
,<xref rid="B210-marinedrugs-17-00320" ref-type="bibr">210</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="marinedrugs-17-00320-t007" orientation="portrait" position="float"><object-id pub-id-type="pii">marinedrugs-17-00320-t007_Table 7</object-id>
<label>Table 7</label>
<caption><p>Serine protease inhibitor metabolites extracted from the database.</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">Molecule Family</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Chemical Classes</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Activity</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Producing Organisms</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Spumigins</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Peptide</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Proteases inhibitory activity</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Nodularia spumigena</italic>
AV1 & CCY 9414,<break></break>
<italic>Anabaena compacta</italic>
NIES-835</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B239-marinedrugs-17-00320" ref-type="bibr">239</xref>
,<xref rid="B240-marinedrugs-17-00320" ref-type="bibr">240</xref>
,<xref rid="B241-marinedrugs-17-00320" ref-type="bibr">241</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cyanopeptolin-like</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Depsipeptide</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Protease inhibitory activity<break></break>
-Other enzyme inhibition<break></break>
-Cytotoxic<break></break>
-Lethal<break></break>
-Antibacterial<break></break>
-Antifungal<break></break>
-Antiprotozoal</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Microcystis</italic>
sp.,<break></break>
<italic>Microcystis aeruginosa</italic>
,<break></break>
<italic>Aphanocapsa</italic>
sp.; <italic>Microchaete loktahensis</italic>
,<break></break>
<italic>Planktothrix agardhii</italic>
,<break></break>
<italic>Scytonema hofmanni</italic>
,<break></break>
<italic>Lyngbya</italic>
sp.,<break></break>
<italic>Lyngbya confervoides</italic>
,<break></break>
<italic>Lyngbya</italic>
spp.,<break></break>
<italic>Lyngbya semiplena</italic>
,<break></break>
<italic>Microcystis viridis</italic>
,<break></break>
<italic>Dichothrix utahensis</italic>
,<break></break>
<italic>Nostoc</italic>
sp.,<break></break>
<italic>Nostoc minutum</italic>
,<break></break>
<italic>Planktothrix rubescens</italic>
,<break></break>
<italic>Lyngbya majuscula</italic>
-<italic>Schizothrix</italic>
sp. (Assemblage),<break></break>
<italic>Stigonema</italic>
sp.,<break></break>
<italic>Symploca</italic>
sp.,<break></break>
<italic>Symploca hydnoides</italic>
,<break></break>
<italic>Nostoc insulare</italic>
</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B30-marinedrugs-17-00320" ref-type="bibr">30</xref>
,<xref rid="B31-marinedrugs-17-00320" ref-type="bibr">31</xref>
,<xref rid="B159-marinedrugs-17-00320" ref-type="bibr">159</xref>
,<xref rid="B185-marinedrugs-17-00320" ref-type="bibr">185</xref>
,<xref rid="B186-marinedrugs-17-00320" ref-type="bibr">186</xref>
,<xref rid="B188-marinedrugs-17-00320" ref-type="bibr">188</xref>
,<xref rid="B243-marinedrugs-17-00320" ref-type="bibr">243</xref>
,<xref rid="B244-marinedrugs-17-00320" ref-type="bibr">244</xref>
,<xref rid="B245-marinedrugs-17-00320" ref-type="bibr">245</xref>
,<xref rid="B246-marinedrugs-17-00320" ref-type="bibr">246</xref>
,<xref rid="B247-marinedrugs-17-00320" ref-type="bibr">247</xref>
,<xref rid="B248-marinedrugs-17-00320" ref-type="bibr">248</xref>
,<xref rid="B249-marinedrugs-17-00320" ref-type="bibr">249</xref>
,<xref rid="B250-marinedrugs-17-00320" ref-type="bibr">250</xref>
,<xref rid="B251-marinedrugs-17-00320" ref-type="bibr">251</xref>
,<xref rid="B252-marinedrugs-17-00320" ref-type="bibr">252</xref>
,<xref rid="B253-marinedrugs-17-00320" ref-type="bibr">253</xref>
,<xref rid="B254-marinedrugs-17-00320" ref-type="bibr">254</xref>
,<xref rid="B255-marinedrugs-17-00320" ref-type="bibr">255</xref>
,<xref rid="B256-marinedrugs-17-00320" ref-type="bibr">256</xref>
,<xref rid="B257-marinedrugs-17-00320" ref-type="bibr">257</xref>
,<xref rid="B258-marinedrugs-17-00320" ref-type="bibr">258</xref>
,<xref rid="B259-marinedrugs-17-00320" ref-type="bibr">259</xref>
,<xref rid="B260-marinedrugs-17-00320" ref-type="bibr">260</xref>
,<xref rid="B261-marinedrugs-17-00320" ref-type="bibr">261</xref>
,<xref rid="B262-marinedrugs-17-00320" ref-type="bibr">262</xref>
,<xref rid="B263-marinedrugs-17-00320" ref-type="bibr">263</xref>
,<xref rid="B264-marinedrugs-17-00320" ref-type="bibr">264</xref>
,<xref rid="B265-marinedrugs-17-00320" ref-type="bibr">265</xref>
,<xref rid="B266-marinedrugs-17-00320" ref-type="bibr">266</xref>
,<xref rid="B267-marinedrugs-17-00320" ref-type="bibr">267</xref>
,<xref rid="B268-marinedrugs-17-00320" ref-type="bibr">268</xref>
,<xref rid="B269-marinedrugs-17-00320" ref-type="bibr">269</xref>
,<xref rid="B270-marinedrugs-17-00320" ref-type="bibr">270</xref>
,<xref rid="B271-marinedrugs-17-00320" ref-type="bibr">271</xref>
,<xref rid="B272-marinedrugs-17-00320" ref-type="bibr">272</xref>
,<xref rid="B273-marinedrugs-17-00320" ref-type="bibr">273</xref>
,<xref rid="B274-marinedrugs-17-00320" ref-type="bibr">274</xref>
,<xref rid="B275-marinedrugs-17-00320" ref-type="bibr">275</xref>
,<xref rid="B276-marinedrugs-17-00320" ref-type="bibr">276</xref>
,<xref rid="B277-marinedrugs-17-00320" ref-type="bibr">277</xref>
,<xref rid="B278-marinedrugs-17-00320" ref-type="bibr">278</xref>
,<xref rid="B279-marinedrugs-17-00320" ref-type="bibr">279</xref>
,<xref rid="B280-marinedrugs-17-00320" ref-type="bibr">280</xref>
,<xref rid="B281-marinedrugs-17-00320" ref-type="bibr">281</xref>
,<xref rid="B282-marinedrugs-17-00320" ref-type="bibr">282</xref>
,<xref rid="B283-marinedrugs-17-00320" ref-type="bibr">283</xref>
,<xref rid="B284-marinedrugs-17-00320" ref-type="bibr">284</xref>
,<xref rid="B285-marinedrugs-17-00320" ref-type="bibr">285</xref>
,<xref rid="B286-marinedrugs-17-00320" ref-type="bibr">286</xref>
,<xref rid="B287-marinedrugs-17-00320" ref-type="bibr">287</xref>
,<xref rid="B288-marinedrugs-17-00320" ref-type="bibr">288</xref>
,<xref rid="B289-marinedrugs-17-00320" ref-type="bibr">289</xref>
,<xref rid="B290-marinedrugs-17-00320" ref-type="bibr">290</xref>
,<xref rid="B291-marinedrugs-17-00320" ref-type="bibr">291</xref>
,<xref rid="B292-marinedrugs-17-00320" ref-type="bibr">292</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Carmaphycins</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Peptide</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Protease inhibition<break></break>
-Cytotoxic<break></break>
-Antiprotozoal</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Symploca</italic>
sp. WHG NAC15/Dec/08–5</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B293-marinedrugs-17-00320" ref-type="bibr">293</xref>
,<xref rid="B294-marinedrugs-17-00320" ref-type="bibr">294</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="marinedrugs-17-00320-t008" orientation="portrait" position="float"><object-id pub-id-type="pii">marinedrugs-17-00320-t008_Table 8</object-id>
<label>Table 8</label>
<caption><p>HDACs inhibitor metabolites extracted from the database.</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">Molecule Family</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Chemical Classes</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Activity</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Producing Organisms</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Largazole</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Depsipeptide</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Histone deacetylases inhibitor<break></break>
-Cytotoxic<break></break>
-Other enzyme inhibition<break></break>
-Pro-drug</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Symploca</italic>
sp.</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B311-marinedrugs-17-00320" ref-type="bibr">311</xref>
,<xref rid="B312-marinedrugs-17-00320" ref-type="bibr">312</xref>
,<xref rid="B313-marinedrugs-17-00320" ref-type="bibr">313</xref>
,<xref rid="B314-marinedrugs-17-00320" ref-type="bibr">314</xref>
,<xref rid="B315-marinedrugs-17-00320" ref-type="bibr">315</xref>
,<xref rid="B316-marinedrugs-17-00320" ref-type="bibr">316</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Santacruzamate A</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Carboxylic acid derived</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Histone deacetylases inhibitor<break></break>
-Cytotoxic</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Symploca</italic>
sp. PAC-19-FEB-10-1</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B317-marinedrugs-17-00320" ref-type="bibr">317</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="marinedrugs-17-00320-t009" orientation="portrait" position="float"><object-id pub-id-type="pii">marinedrugs-17-00320-t009_Table 9</object-id>
<label>Table 9</label>
<caption><p>Anti-inflammatory metabolites extracted from the database.</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">Molecule Family</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Chemical Classes</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Activity</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Producing Organisms</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Aeruginosins</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Peptide</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Anti-inflammatory activity<break></break>
-Protease inhibitor<break></break>
-No cytotoxicity</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Microcystis aeruginosa</italic>
NIES-98, NIES-298, NIES-101, NIES-89. <italic>Microcystis viridis</italic>
NIES-102 <italic>Planktothrix agardhii</italic>
CYA 126/8.<break></break>
<italic>Nodularia spumigena</italic>
CCY9414. <italic>Nostoc</italic>
sp. Lukesova 30/93</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B62-marinedrugs-17-00320" ref-type="bibr">62</xref>
,<xref rid="B321-marinedrugs-17-00320" ref-type="bibr">321</xref>
,<xref rid="B322-marinedrugs-17-00320" ref-type="bibr">322</xref>
,<xref rid="B323-marinedrugs-17-00320" ref-type="bibr">323</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Phycocyanin</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Peptide</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Anti-inflammatory<break></break>
-Antioxidant<break></break>
-Specific inhibitor of COX-2<break></break>
-No lethality</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">All</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B59-marinedrugs-17-00320" ref-type="bibr">59</xref>
,<xref rid="B64-marinedrugs-17-00320" ref-type="bibr">64</xref>
,<xref rid="B324-marinedrugs-17-00320" ref-type="bibr">324</xref>
,<xref rid="B325-marinedrugs-17-00320" ref-type="bibr">325</xref>
,<xref rid="B326-marinedrugs-17-00320" ref-type="bibr">326</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Scytonemin</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Alkaloid</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Anti-inflammatory<break></break>
-Enzyme inhibition<break></break>
-No cytotoxicity</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Stigonema</italic>
sp., <italic>Nostoc punctiforme</italic>
, <italic>Anabaena variabilis</italic>
, <italic>Anabaena ambigua</italic>
, <italic>Aphanocapsa/Synechocystis</italic>
sp. (assembly), <italic>Aulosira fertilissima</italic>
, <italic>Calothrix</italic>
sp., <italic>Calothrix parietina</italic>
, <italic>Calothrix crustacea</italic>
, <italic>Chlorogloeopsis</italic>
sp., <italic>Chroococcidiopsis</italic>
sp., <italic>Chroococcus</italic>
sp.; <italic>Cylindrospermum</italic>
sp., <italic>Diplocolon</italic>
sp., <italic>Entophysalis granulos</italic>
, <italic>Gloeocapsa</italic>
sp., <italic>Hapalosiphon</italic>
sp., <italic>Hapalosiphon fontinalis</italic>
; <italic>Lyngbya</italic>
sp.,<break></break>
<italic>Lyngbya aestuarii</italic>
, <italic>Nostoc parmelioides</italic>
, <italic>Nostoc commune</italic>
, <italic>Nostoc microscopium</italic>
, <italic>Nostoc pruniforme</italic>
, <italic>Phormidium</italic>
sp., <italic>Pleurocapsa</italic>
sp., <italic>Rivularia</italic>
atra, <italic>Rivularia</italic>
sp., <italic>Schizothrix</italic>
sp., <italic>Scytonema</italic>
sp., <italic>Tolyothrix</italic>
sp., <italic>Tolypothrix tenni</italic>
, <italic>Westiellopsis prolifica</italic>
, <italic>Scytonema hoffmani</italic>
</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B65-marinedrugs-17-00320" ref-type="bibr">65</xref>
,<xref rid="B327-marinedrugs-17-00320" ref-type="bibr">327</xref>
,<xref rid="B328-marinedrugs-17-00320" ref-type="bibr">328</xref>
,<xref rid="B329-marinedrugs-17-00320" ref-type="bibr">329</xref>
,<xref rid="B330-marinedrugs-17-00320" ref-type="bibr">330</xref>
,<xref rid="B331-marinedrugs-17-00320" ref-type="bibr">331</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="marinedrugs-17-00320-t010" orientation="portrait" position="float"><object-id pub-id-type="pii">marinedrugs-17-00320-t010_Table 10</object-id>
<label>Table 10</label>
<caption><p>Antioxidant metabolites extracted from the database.</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">Molecule Family</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Chemical Classes</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Activity</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Producing Organisms</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><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">Terpenoid</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Antioxidant<break></break>
-Sunscreen</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">All</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B56-marinedrugs-17-00320" ref-type="bibr">56</xref>
,<xref rid="B345-marinedrugs-17-00320" ref-type="bibr">345</xref>
,<xref rid="B346-marinedrugs-17-00320" ref-type="bibr">346</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Chlorophylls</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Chlorin</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Photosynthesis<break></break>
-Antioxidant<break></break>
-Pro-oxidant (sensitizer for singlet oxygen production)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">All</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B57-marinedrugs-17-00320" ref-type="bibr">57</xref>
,<xref rid="B345-marinedrugs-17-00320" ref-type="bibr">345</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MAAs</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Cyclohexenone linked with an amino acid</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Antioxidant<break></break>
-Sunscreens</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Synechocystis</italic>
sp. PCC 6803, <italic>Gloeocapsa</italic>
sp. CU-2556, <italic>Aphanothece halophytica</italic>
, <italic>Gloeocapsa</italic>
sp., <italic>Euhalothece</italic>
sp., <italic>Microcystis aeruginosa</italic>
, <italic>Arthrospira</italic>
sp. CU2556, <italic>Lyngbya</italic>
sp. CU2555, <italic>Leptolyngbya</italic>
sp., <italic>Phormidium</italic>
sp., <italic>Lyngbya</italic>
cf. <italic>aestuarii</italic>
, <italic>Microcoleus chthonoplastes</italic>
, <italic>Microcoleus</italic>
sp., <italic>Oscillatoria spongelidae</italic>
, <italic>Trichodesmium</italic>
spp., <italic>Anabaena</italic>
sp., <italic>Anabaena doliolum</italic>
, <italic>Anabaena variabilis</italic>
PCC 7937, <italic>Nostoc</italic>
sp., <italic>Nostoc commune</italic>
var. Vaucher, <italic>Nostoc commune</italic>
, <italic>Scytonema</italic>
sp., <italic>Nostoc punctiforme</italic>
ATCC 29133, <italic>Nostoc</italic>
sp. HKAR-2 and HKAR-6, <italic>Nodularia baltica</italic>
, <italic>Nodularia harveyana</italic>
, <italic>Nodularia spumigena</italic>
, <italic>Aphanizomenon flos-aquae</italic>
, <italic>Chlorogloeopsis</italic>
PCC 6912</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B58-marinedrugs-17-00320" ref-type="bibr">58</xref>
,<xref rid="B345-marinedrugs-17-00320" ref-type="bibr">345</xref>
,<xref rid="B347-marinedrugs-17-00320" ref-type="bibr">347</xref>
,<xref rid="B348-marinedrugs-17-00320" ref-type="bibr">348</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Phycocyanin</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Peptide</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Anti-inflammatory<break></break>
-Antioxidant<break></break>
-Specific inhibitor of COX-2<break></break>
-No lethality</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">All</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B59-marinedrugs-17-00320" ref-type="bibr">59</xref>
,<xref rid="B64-marinedrugs-17-00320" ref-type="bibr">64</xref>
,<xref rid="B324-marinedrugs-17-00320" ref-type="bibr">324</xref>
,<xref rid="B325-marinedrugs-17-00320" ref-type="bibr">325</xref>
,<xref rid="B326-marinedrugs-17-00320" ref-type="bibr">326</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="marinedrugs-17-00320-t011" orientation="portrait" position="float"><object-id pub-id-type="pii">marinedrugs-17-00320-t011_Table 11</object-id>
<label>Table 11</label>
<caption><p>Other metabolites extracted from our database with promising biomedical potential.</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">Molecule Family</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Chemical Classes</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Activity</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Producing Organisms</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">References</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Grassystatins-Tasiamides</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Depsipeptide</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-Protease inhibitory activity<break></break>
-Cytotoxic<break></break>
-Reduce antigen presentation in dendritic cells</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Lyngbya confervoides</italic>
,<break></break>
<italic>Symploca</italic>
sp.,<break></break>
<italic>Symploca</italic>
sp. NHI304,<break></break>
<italic>Lyngbya</italic>
sp. NIH399</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B350-marinedrugs-17-00320" ref-type="bibr">350</xref>
,<xref rid="B351-marinedrugs-17-00320" ref-type="bibr">351</xref>
,<xref rid="B352-marinedrugs-17-00320" ref-type="bibr">352</xref>
,<xref rid="B353-marinedrugs-17-00320" ref-type="bibr">353</xref>
,<xref rid="B354-marinedrugs-17-00320" ref-type="bibr">354</xref>
,<xref rid="B355-marinedrugs-17-00320" ref-type="bibr">355</xref>
,<xref rid="B356-marinedrugs-17-00320" ref-type="bibr">356</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Columbamides</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Acyl amide</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">-CB1 and CB2 ligands</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"><italic>Moorea bouillonii</italic>
PNG05-198</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B363-marinedrugs-17-00320" ref-type="bibr">363</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
</floats-group>
</pmc>
<affiliations><list></list>
<tree><noCountry><name sortKey="Bernard, Cecile" sort="Bernard, Cecile" uniqKey="Bernard C" first="Cécile" last="Bernard">Cécile Bernard</name>
<name sortKey="Demay, Justine" sort="Demay, Justine" uniqKey="Demay J" first="Justine" last="Demay">Justine Demay</name>
<name sortKey="Marie, Benjamin" sort="Marie, Benjamin" uniqKey="Marie B" first="Benjamin" last="Marie">Benjamin Marie</name>
<name sortKey="Reinhardt, Anita" sort="Reinhardt, Anita" uniqKey="Reinhardt A" first="Anita" last="Reinhardt">Anita Reinhardt</name>
</noCountry>
</tree>
</affiliations>
</record>
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