Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics
Identifieur interne : 000141 ( Pmc/Curation ); précédent : 000140; suivant : 000142Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics
Auteurs : Tomàs Llorens-Marès [Espagne] ; Shibu Yooseph [États-Unis] ; Johannes Goll [États-Unis] ; Jeff Hoffman [États-Unis] ; Maria Vila-Costa [Espagne] ; Carles M. Borrego [Espagne] ; Chris L. Dupont [États-Unis] ; Emilio O. Casamayor [Espagne]Source :
- The ISME Journal [ 1751-7362 ] ; 2015.
Abstract
Stratified sulfurous lakes are appropriate environments for studying the links between composition and functionality in microbial communities and are potentially modern analogs of anoxic conditions prevailing in the ancient ocean. We explored these aspects in the Lake Banyoles karstic area (NE Spain) through metagenomics and
Url:
DOI: 10.1038/ismej.2014.254
PubMed: 25575307
PubMed Central: 4478705
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<author><name sortKey="Llorens Mares, Tomas" sort="Llorens Mares, Tomas" uniqKey="Llorens Mares T" first="Tomàs" last="Llorens-Marès">Tomàs Llorens-Marès</name>
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<author><name sortKey="Casamayor, Emilio O" sort="Casamayor, Emilio O" uniqKey="Casamayor E" first="Emilio O" last="Casamayor">Emilio O. Casamayor</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics</title>
<author><name sortKey="Llorens Mares, Tomas" sort="Llorens Mares, Tomas" uniqKey="Llorens Mares T" first="Tomàs" last="Llorens-Marès">Tomàs Llorens-Marès</name>
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<country xml:lang="fr">Espagne</country>
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<author><name sortKey="Yooseph, Shibu" sort="Yooseph, Shibu" uniqKey="Yooseph S" first="Shibu" last="Yooseph">Shibu Yooseph</name>
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, San Diego, CA,<country>USA</country>
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<country xml:lang="fr">États-Unis</country>
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<author><name sortKey="Goll, Johannes" sort="Goll, Johannes" uniqKey="Goll J" first="Johannes" last="Goll">Johannes Goll</name>
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, Rockville, MD,<country>USA</country>
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, San Diego, CA,<country>USA</country>
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<country xml:lang="fr">États-Unis</country>
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<author><name sortKey="Vila Costa, Maria" sort="Vila Costa, Maria" uniqKey="Vila Costa M" first="Maria" last="Vila-Costa">Maria Vila-Costa</name>
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, Girona,<country>Spain</country>
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<author><name sortKey="Borrego, Carles M" sort="Borrego, Carles M" uniqKey="Borrego C" first="Carles M" last="Borrego">Carles M. Borrego</name>
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<author><name sortKey="Dupont, Chris L" sort="Dupont, Chris L" uniqKey="Dupont C" first="Chris L" last="Dupont">Chris L. Dupont</name>
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, San Diego, CA,<country>USA</country>
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<author><name sortKey="Casamayor, Emilio O" sort="Casamayor, Emilio O" uniqKey="Casamayor E" first="Emilio O" last="Casamayor">Emilio O. Casamayor</name>
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, Girona,<country>Spain</country>
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<series><title level="j">The ISME Journal</title>
<idno type="ISSN">1751-7362</idno>
<idno type="eISSN">1751-7370</idno>
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<front><div type="abstract" xml:lang="en"><p>Stratified sulfurous lakes are appropriate environments for studying the links between composition and functionality in microbial communities and are potentially modern analogs of anoxic conditions prevailing in the ancient ocean. We explored these aspects in the Lake Banyoles karstic area (NE Spain) through metagenomics and <italic>in silico</italic>
reconstruction of carbon, nitrogen and sulfur metabolic pathways that were tightly coupled through a few bacterial groups. The potential for nitrogen fixation and denitrification was detected in both autotrophs and heterotrophs, with a major role for nitrogen and carbon fixations in <italic>Chlorobiaceae</italic>
. <italic>Campylobacterales</italic>
accounted for a large percentage of denitrification genes, while <italic>Gallionellales</italic>
were putatively involved in denitrification, iron oxidation and carbon fixation and may have a major role in the biogeochemistry of the iron cycle. <italic>Bacteroidales</italic>
were also abundant and showed potential for dissimilatory nitrate reduction to ammonium. The very low abundance of genes for nitrification, the minor presence of anammox genes, the high potential for nitrogen fixation and mineralization and the potential for chemotrophic CO<sub>2</sub>
fixation and CO oxidation all provide potential clues on the anoxic zones functioning. We observed higher gene abundance of ammonia-oxidizing bacteria than ammonia-oxidizing archaea that may have a geochemical and evolutionary link related to the dominance of Fe in these environments. Overall, these results offer a more detailed perspective on the microbial ecology of anoxic environments and may help to develop new geochemical proxies to infer biology and chemistry interactions in ancient ecosystems.</p>
</div>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">ISME J</journal-id>
<journal-id journal-id-type="iso-abbrev">ISME J</journal-id>
<journal-title-group><journal-title>The ISME Journal</journal-title>
</journal-title-group>
<issn pub-type="ppub">1751-7362</issn>
<issn pub-type="epub">1751-7370</issn>
<publisher><publisher-name>Nature Publishing Group</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25575307</article-id>
<article-id pub-id-type="pmc">4478705</article-id>
<article-id pub-id-type="pii">ismej2014254</article-id>
<article-id pub-id-type="doi">10.1038/ismej.2014.254</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Original Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Connecting biodiversity and potential functional role in modern euxinic environments by microbial metagenomics</article-title>
<alt-title alt-title-type="running">Biodiversity and biogeochemistry in euxinic lakes</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Llorens-Marès</surname>
<given-names>Tomàs</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Yooseph</surname>
<given-names>Shibu</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Goll</surname>
<given-names>Johannes</given-names>
</name>
<xref ref-type="aff" rid="aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hoffman</surname>
<given-names>Jeff</given-names>
</name>
<xref ref-type="aff" rid="aff4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Vila-Costa</surname>
<given-names>Maria</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Borrego</surname>
<given-names>Carles M</given-names>
</name>
<xref ref-type="aff" rid="aff5">5</xref>
<xref ref-type="aff" rid="aff6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dupont</surname>
<given-names>Chris L</given-names>
</name>
<xref ref-type="aff" rid="aff4">4</xref>
<xref ref-type="corresp" rid="caf1">*</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Casamayor</surname>
<given-names>Emilio O</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="corresp" rid="caf1">*</xref>
</contrib>
<aff id="aff1"><label>1</label>
<institution>Integrative Freshwater Ecology Group, Center of Advanced Studies of Blanes–Spanish Council for Research (CEAB-CSIC), Blanes</institution>
, Girona,<country>Spain</country>
</aff>
<aff id="aff2"><label>2</label>
<institution>Informatics Group, J Craig Venter Institute</institution>
, San Diego, CA,<country>USA</country>
</aff>
<aff id="aff3"><label>3</label>
<institution>Informatics Group, J Craig Venter Institute</institution>
, Rockville, MD,<country>USA</country>
</aff>
<aff id="aff4"><label>4</label>
<institution>Microbial and Environmental Genomics Group, J Craig Venter Institute</institution>
, San Diego, CA,<country>USA</country>
</aff>
<aff id="aff5"><label>5</label>
<institution>Water Quality and Microbial Diversity, Catalan Institute for Water Research (ICRA)</institution>
, Girona,<country>Spain</country>
</aff>
<aff id="aff6"><label>6</label>
<institution>Group of Molecular Microbial Ecology, Institute of Aquatic Ecology, University of Girona</institution>
, Girona,<country>Spain</country>
</aff>
</contrib-group>
<author-notes><corresp id="caf1"><label>*</label>
<institution>Integrative Freshwater Ecology Group, Center of Advanced Studies of Blanes–Spanish Council for Research (CEAB-CSIC)</institution>
, Accés Cala Sant Francesc, 14, Blanes, Girona 17300, <country>Spain</country>
. E-mail: <email>casamayor@ceab.csic.es</email>
or <institution>Microbial and Environmental Genomics Group, J Craig Venter Institute</institution>
, San Diego, CA 92037, <country>USA</country>
. E-mail: <email>cdupont@jcvi.org</email>
</corresp>
</author-notes>
<pub-date pub-type="ppub"><month>07</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="epub"><day>09</day>
<month>01</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>1</day>
<month>7</month>
<year>2015</year>
</pub-date>
<volume>9</volume>
<issue>7</issue>
<fpage>1648</fpage>
<lpage>1661</lpage>
<history><date date-type="received"><day>19</day>
<month>03</month>
<year>2014</year>
</date>
<date date-type="rev-recd"><day>17</day>
<month>11</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>24</day>
<month>11</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2015 International Society for Microbial Ecology</copyright-statement>
<copyright-year>2015</copyright-year>
<copyright-holder>International Society for Microbial Ecology</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/">http://creativecommons.org/licenses/by-nc-nd/3.0/</ext-link>
</license-p>
</license>
</permissions>
<abstract><p>Stratified sulfurous lakes are appropriate environments for studying the links between composition and functionality in microbial communities and are potentially modern analogs of anoxic conditions prevailing in the ancient ocean. We explored these aspects in the Lake Banyoles karstic area (NE Spain) through metagenomics and <italic>in silico</italic>
reconstruction of carbon, nitrogen and sulfur metabolic pathways that were tightly coupled through a few bacterial groups. The potential for nitrogen fixation and denitrification was detected in both autotrophs and heterotrophs, with a major role for nitrogen and carbon fixations in <italic>Chlorobiaceae</italic>
. <italic>Campylobacterales</italic>
accounted for a large percentage of denitrification genes, while <italic>Gallionellales</italic>
were putatively involved in denitrification, iron oxidation and carbon fixation and may have a major role in the biogeochemistry of the iron cycle. <italic>Bacteroidales</italic>
were also abundant and showed potential for dissimilatory nitrate reduction to ammonium. The very low abundance of genes for nitrification, the minor presence of anammox genes, the high potential for nitrogen fixation and mineralization and the potential for chemotrophic CO<sub>2</sub>
fixation and CO oxidation all provide potential clues on the anoxic zones functioning. We observed higher gene abundance of ammonia-oxidizing bacteria than ammonia-oxidizing archaea that may have a geochemical and evolutionary link related to the dominance of Fe in these environments. Overall, these results offer a more detailed perspective on the microbial ecology of anoxic environments and may help to develop new geochemical proxies to infer biology and chemistry interactions in ancient ecosystems.</p>
</abstract>
</article-meta>
</front>
<floats-group><fig id="fig1"><label>Figure 1</label>
<caption><p>Vertical profiles of physicochemical data for Lake Banyoles basin C-III and Lake Cisó. Metagenomic analyses were carried out at two selected depths (dotted lines): the oxic–anoxic interface (shadowed areas indicate the redoxcline zone) and the anoxic and sulfurous (euxinic) hypolimnia.</p>
</caption>
<graphic xlink:href="ismej2014254f1"></graphic>
</fig>
<fig id="fig2"><label>Figure 2</label>
<caption><p>Prokaryotic community structure (relative abundances at the Order level) of Lake Banyoles basin C-III and Lake Cisó obtained from the 16S rRNA gene present in the metagenomic pool. See detailed information in <xref ref-type="supplementary-material" rid="sup1">Supplementary Table S2</xref>
. Hierarchical clustering based on Bray–Curtis dissimilarity matrices.</p>
</caption>
<graphic xlink:href="ismej2014254f2"></graphic>
</fig>
<fig id="fig3"><label>Figure 3</label>
<caption><p>Heatmap plot and functional clustering of the selected KEGG Orthologs for the predicted open reading frames (ORFs) from the metagenomic reads for Lake Cisó and Banyoles basin C-III.</p>
</caption>
<graphic xlink:href="ismej2014254f3"></graphic>
</fig>
<fig id="fig4"><label>Figure 4</label>
<caption><p>Genetic potential for several steps of the carbon cycle in Lake Cisó and Banyoles basin C-III using a combination of normalized marker genes. Arrow size proportional to the potential flux of the carbon pathways (100% value, see <xref ref-type="supplementary-material" rid="sup1">Supplementary Table S3</xref>
). Dotted lines: not detected marked genes but putative presence of the pathway (see main text). Relative abundances for the main microbes potentially driving each conversion step are shown (only for those that contributed >1% of the marker genes mixture). *<italic>Chromatiales</italic>
: anoxygenic phototrophy through the Calvin cycle.</p>
</caption>
<graphic xlink:href="ismej2014254f4"></graphic>
</fig>
<fig id="fig5"><label>Figure 5</label>
<caption><p>Genetic potential for several steps of the nitrogen cycle in Lake Cisó and Banyoles basin C-III using a combination of normalized marker genes. Arrow size proportional to the potential flux of the nitrogen pathways (100% value, see <xref ref-type="supplementary-material" rid="sup1">Supplementary Table S3</xref>
). Dotted lines: not detected marked genes but putative presence of the pathway (see main text). Relative abundances for the main microbes potentially driving each conversion step are shown (only for those that contributed >1% of the marker genes mixture). **Presence of AOA, AOB and nitrite-oxidizing bacteria (NOB) reads in the metagenomic pool.</p>
</caption>
<graphic xlink:href="ismej2014254f5"></graphic>
</fig>
<fig id="fig6"><label>Figure 6</label>
<caption><p>Genetic potential for several steps of the sulfur cycle in Lake Cisó and Banyoles basin C-III using a combination of normalized marker genes. Arrow size proportional to the potential flux of the sulfur pathways (100% value, see <xref ref-type="supplementary-material" rid="sup1">Supplementary Table S3</xref>
). Relative abundances for the main microbes potentially driving each conversion step are shown (only for those that contributed >1% of the marker genes mixture). **<italic>Campylobacteraceae</italic>
contributed through <italic>sox</italic>
genes not reported in KEGG database.</p>
</caption>
<graphic xlink:href="ismej2014254f6"></graphic>
</fig>
<fig id="fig7"><label>Figure 7</label>
<caption><p>Lake Cisó and basin C-III of Lake Banyoles as modern analogs of anoxic conditions prevailing in the ancient ocean. The illustration shows the geochemical distributions of Fe, S, C and O<sub>2</sub>
in depth profiles and along different oceanic regimes (shelf, slope, open ocean) during Proterozoic (<xref ref-type="bibr" rid="bib35">Lyons <italic>et al.,</italic>
2014</xref>
). Lake Cisó would be closer to coastal and continental shelf areas, whereas Banyoles C-III would be a more open ocean analogue.</p>
</caption>
<graphic xlink:href="ismej2014254f7"></graphic>
</fig>
<table-wrap id="tbl1"><label>Table 1</label>
<caption><title>Biogeochemical data for Lake Cisó and Banyoles basin C-III</title>
</caption>
<table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
</colgroup>
<thead valign="bottom"><tr><th align="left" valign="top" charoff="50"> </th>
<th align="center" valign="top" charoff="50"><italic>Cisó ML</italic>
</th>
<th align="center" valign="top" charoff="50"><italic>Cisó HL</italic>
</th>
<th align="center" valign="top" charoff="50"><italic>C-III ML</italic>
</th>
<th align="center" valign="top" charoff="50"><italic>C-III HL</italic>
</th>
</tr>
</thead>
<tbody valign="top"><tr><td align="left" valign="top" charoff="50">Depth (m)</td>
<td align="center" valign="top" charoff="50">1.75</td>
<td align="center" valign="top" charoff="50">4.5</td>
<td align="center" valign="top" charoff="50">22.25</td>
<td align="center" valign="top" charoff="50">24</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Temperature (°C)</td>
<td align="center" valign="top" charoff="50">12.9</td>
<td align="center" valign="top" charoff="50">10.6</td>
<td align="center" valign="top" charoff="50">12.6</td>
<td align="center" valign="top" charoff="50">12.6</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Conductivity (μS cm<sup>-1</sup>
)</td>
<td align="center" valign="top" charoff="50">2260</td>
<td align="center" valign="top" charoff="50">2268</td>
<td align="center" valign="top" charoff="50">2603</td>
<td align="center" valign="top" charoff="50">2604</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Eh (mV)</td>
<td align="center" valign="top" charoff="50">−30</td>
<td align="center" valign="top" charoff="50">−86</td>
<td align="center" valign="top" charoff="50">195</td>
<td align="center" valign="top" charoff="50">145</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Oxygen (mg l<sup>−1</sup>
)</td>
<td align="center" valign="top" charoff="50">0.10</td>
<td align="center" valign="top" charoff="50">0</td>
<td align="center" valign="top" charoff="50">0.25</td>
<td align="center" valign="top" charoff="50">0</td>
</tr>
<tr><td align="left" valign="top" charoff="50">H<sub>2</sub>
S (μ<sc>M</sc>
)</td>
<td align="center" valign="top" charoff="50">12.8</td>
<td align="center" valign="top" charoff="50">531.9</td>
<td align="center" valign="top" charoff="50">0.8</td>
<td align="center" valign="top" charoff="50">3.6</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Light (% incident)</td>
<td align="center" valign="top" charoff="50">1%</td>
<td align="center" valign="top" charoff="50"><0.1%</td>
<td align="center" valign="top" charoff="50">1%</td>
<td align="center" valign="top" charoff="50"><0.1%</td>
</tr>
<tr><td align="left" valign="top" charoff="50">TOC (mg l<sup>−1</sup>
)</td>
<td align="center" valign="top" charoff="50">5</td>
<td align="center" valign="top" charoff="50">3</td>
<td align="center" valign="top" charoff="50">1.5</td>
<td align="center" valign="top" charoff="50">3</td>
</tr>
<tr><td align="left" valign="top" charoff="50">pH</td>
<td align="center" valign="top" charoff="50">7.40</td>
<td align="center" valign="top" charoff="50">7.23</td>
<td align="center" valign="top" charoff="50">7.14</td>
<td align="center" valign="top" charoff="50">7.15</td>
</tr>
<tr><td align="left" valign="top" charoff="50">TDP (μ<sc>M</sc>
)</td>
<td align="center" valign="top" charoff="50">1.05</td>
<td align="center" valign="top" charoff="50">2.83</td>
<td align="center" valign="top" charoff="50">0.33</td>
<td align="center" valign="top" charoff="50">0.37</td>
</tr>
<tr><td align="left" valign="top" charoff="50">NH<sub>4</sub>
(μ<sc>M</sc>
)</td>
<td align="center" valign="top" charoff="50">44.39</td>
<td align="center" valign="top" charoff="50">50.99</td>
<td align="center" valign="top" charoff="50">25.04</td>
<td align="center" valign="top" charoff="50">37.52</td>
</tr>
<tr><td align="left" valign="top" charoff="50">NO<sub>2</sub>
(μ<sc>M</sc>
)</td>
<td align="center" valign="top" charoff="50">0.75</td>
<td align="center" valign="top" charoff="50">b.d.l.</td>
<td align="center" valign="top" charoff="50">0.21</td>
<td align="center" valign="top" charoff="50">0.00</td>
</tr>
<tr><td align="left" valign="top" charoff="50">NO<sub>3</sub>
(μ<sc>M</sc>
)</td>
<td align="center" valign="top" charoff="50">2.20</td>
<td align="center" valign="top" charoff="50">1.44</td>
<td align="center" valign="top" charoff="50">6.20</td>
<td align="center" valign="top" charoff="50">0.54</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Urea (μ<sc>M</sc>
)</td>
<td align="center" valign="top" charoff="50">4.84</td>
<td align="center" valign="top" charoff="50">0.17</td>
<td align="center" valign="top" charoff="50">1.91</td>
<td align="center" valign="top" charoff="50">1.08</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Si (μ<sc>M</sc>
)</td>
<td align="center" valign="top" charoff="50">185.0</td>
<td align="center" valign="top" charoff="50">168.1</td>
<td align="center" valign="top" charoff="50">144.8</td>
<td align="center" valign="top" charoff="50">114.5</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Chl <italic>a</italic>
(μg l<sup>−1</sup>
)</td>
<td align="center" valign="top" charoff="50">1.7</td>
<td align="center" valign="top" charoff="50">22.5</td>
<td align="center" valign="top" charoff="50">1.1</td>
<td align="center" valign="top" charoff="50">0.8</td>
</tr>
<tr><td align="left" valign="top" charoff="50">BChl <italic>a</italic>
(μg l<sup>−1</sup>
)</td>
<td align="center" valign="top" charoff="50">2.4</td>
<td align="center" valign="top" charoff="50">123.7</td>
<td align="center" valign="top" charoff="50">1.1</td>
<td align="center" valign="top" charoff="50">1.6</td>
</tr>
<tr><td align="left" valign="top" charoff="50">BChl <italic>c</italic>
and <italic>d</italic>
(μg l<sup>−1</sup>
)</td>
<td align="center" valign="top" charoff="50">5.4</td>
<td align="center" valign="top" charoff="50">39.3</td>
<td align="center" valign="top" charoff="50">0</td>
<td align="center" valign="top" charoff="50">0</td>
</tr>
<tr><td align="left" valign="top" charoff="50">BChl <italic>e</italic>
(μg l<sup>−1</sup>
)</td>
<td align="center" valign="top" charoff="50">0.8</td>
<td align="center" valign="top" charoff="50">13.6</td>
<td align="center" valign="top" charoff="50">25.8</td>
<td align="center" valign="top" charoff="50">40.6</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="t1-fn1"><p>Abbreviations: BChl, bacteriochlorophyll; b.d.l., below detection limits; Chl<italic>a</italic>
, chlorophyll <italic>a</italic>
; HL, hypolimnion; Eh, redox potential; ML, metalimnion; TOC, total organic carbon; TDP, total dissolved phosphorus.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="tbl2"><label>Table 2</label>
<caption><title>Total number of metagenomic reads (averaged c. 1 million per sample) for Lake Cisó and Banyoles basin C-III</title>
</caption>
<table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
</colgroup>
<thead valign="bottom"><tr><th align="left" valign="top" charoff="50"> </th>
<th align="center" valign="top" charoff="50"><italic>Cisó ML</italic>
</th>
<th align="center" valign="top" charoff="50"><italic>Cisó HL</italic>
</th>
<th align="center" valign="top" charoff="50"><italic>C-III ML</italic>
</th>
<th align="center" valign="top" charoff="50"><italic>C-III HL</italic>
</th>
</tr>
</thead>
<tbody valign="top"><tr><td align="left" valign="top" charoff="50">Total number of reads</td>
<td align="center" valign="top" charoff="50">869 947</td>
<td align="center" valign="top" charoff="50">991 056</td>
<td align="center" valign="top" charoff="50">1 071 206</td>
<td align="center" valign="top" charoff="50">1 077 431</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic>Taxonomically assigned reads (%)</italic>
</td>
<td align="center" valign="top" charoff="50">46.7</td>
<td align="center" valign="top" charoff="50">53.5</td>
<td align="center" valign="top" charoff="50">54.2</td>
<td align="center" valign="top" charoff="50">62.4</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> <italic>Bacteria</italic>
(%)</td>
<td align="center" valign="top" charoff="50">92.5</td>
<td align="center" valign="top" charoff="50">94.6</td>
<td align="center" valign="top" charoff="50">91.9</td>
<td align="center" valign="top" charoff="50">93.7</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> <italic>Archaea</italic>
(%)</td>
<td align="center" valign="top" charoff="50">0.7</td>
<td align="center" valign="top" charoff="50">3.5</td>
<td align="center" valign="top" charoff="50">1.4</td>
<td align="center" valign="top" charoff="50">1.7</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> <italic>Eukarya</italic>
(%)</td>
<td align="center" valign="top" charoff="50">2.8</td>
<td align="center" valign="top" charoff="50">1.1</td>
<td align="center" valign="top" charoff="50">2.7</td>
<td align="center" valign="top" charoff="50">0.7</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses (%)</td>
<td align="center" valign="top" charoff="50">4.0</td>
<td align="center" valign="top" charoff="50">0.8</td>
<td align="center" valign="top" charoff="50">4.0</td>
<td align="center" valign="top" charoff="50">3.9</td>
</tr>
<tr><td align="left" valign="top" charoff="50"><italic>16S rRNA genes in the metagenomic pool</italic>
</td>
<td align="center" valign="top" charoff="50">465</td>
<td align="center" valign="top" charoff="50">578</td>
<td align="center" valign="top" charoff="50">690</td>
<td align="center" valign="top" charoff="50">787</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> <italic>Bacteria</italic>
(%)</td>
<td align="center" valign="top" charoff="50">99.6</td>
<td align="center" valign="top" charoff="50">97.9</td>
<td align="center" valign="top" charoff="50">100</td>
<td align="center" valign="top" charoff="50">99.4</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> <italic>Archaea</italic>
(%)</td>
<td align="center" valign="top" charoff="50">0.4</td>
<td align="center" valign="top" charoff="50">2.1</td>
<td align="center" valign="top" charoff="50">0</td>
<td align="center" valign="top" charoff="50">0.6</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Functionally assigned metagenomic reads (%)</td>
<td align="center" valign="top" charoff="50">25.8</td>
<td align="center" valign="top" charoff="50">27.5</td>
<td align="center" valign="top" charoff="50">30.5</td>
<td align="center" valign="top" charoff="50">32.6</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Reads of key genes in C, N and S cycles</td>
<td align="center" valign="top" charoff="50">2392</td>
<td align="center" valign="top" charoff="50">3574</td>
<td align="center" valign="top" charoff="50">4773</td>
<td align="center" valign="top" charoff="50">5162</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="t2-fn1"><p>Abbreviations: HL, hypolimnion; ML, metalimnion.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="tbl3"><label>Table 3</label>
<caption><title>Carbon fixation cycles and main metabolic traits of the C-fixing microorganisms found in this study</title>
</caption>
<table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col>
<col align="left"></col>
<col align="left"></col>
<col align="left"></col>
</colgroup>
<thead valign="bottom"><tr><th align="left" valign="top" charoff="50"><italic>Taxa/phylogeny</italic>
</th>
<th align="left" valign="top" charoff="50"><italic>C-fixation pathway</italic>
</th>
<th align="left" valign="top" charoff="50"><italic>Traits</italic>
</th>
<th align="center" valign="top" charoff="50"><italic>Main genera identified in Lakes Cisó and C-III from the 16S rRNA gene present in the metagenomic pool</italic>
</th>
</tr>
</thead>
<tbody valign="top"><tr><td align="left" valign="top" charoff="50">Gallionellales
<italic>Betaproteobacteria</italic>
</td>
<td align="left" valign="top" charoff="50">Calvin</td>
<td align="left" valign="top" charoff="50">Facultative
Chemolithoautotroph
Energy sources: Fe(II)/sulfide
Denitrification</td>
<td align="left" valign="top" charoff="50"><italic>Sideroxydans</italic>
</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Hydrogenophilales
<italic>Betaproteobacteria</italic>
</td>
<td align="left" valign="top" charoff="50">Calvin</td>
<td align="left" valign="top" charoff="50">Chemolithoautotroph
Sulfide oxidation</td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
<tr><td align="left" valign="top" charoff="50">Campylobacterales
<italic>Epsilonproteobacteria</italic>
</td>
<td align="left" valign="top" charoff="50">Arnon<xref ref-type="fn" rid="t3-fn2">a</xref>
</td>
<td align="left" valign="top" charoff="50">Chemolithoautotroph
Denitrification
Sulfide oxidation</td>
<td align="left" valign="top" charoff="50"><italic>Arcobacter, Sulfuricurvum, Sulfurimonas</italic>
</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Chromatiales
<italic>Gammaproteobacteria</italic>
</td>
<td align="left" valign="top" charoff="50">Calvin</td>
<td align="left" valign="top" charoff="50">Photolithoautotroph Anaerobic
Tolerates oxygen</td>
<td align="left" valign="top" charoff="50"><italic>Lamprocystis</italic>
</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Chlorobiales
<italic>Chlorobi</italic>
</td>
<td align="left" valign="top" charoff="50">Arnon<xref ref-type="fn" rid="t3-fn2">a</xref>
</td>
<td align="left" valign="top" charoff="50">Photolithoautotroph
Anaerobic (strict)
N fixation</td>
<td align="left" valign="top" charoff="50"><italic>Chlorobium luteolum</italic>
</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Desulfobacterales
<italic>Deltaproteobacteria</italic>
</td>
<td align="left" valign="top" charoff="50">Arnon<xref ref-type="fn" rid="t3-fn2">a</xref>
Reductive acetyl-CoA<xref ref-type="fn" rid="t3-fn3">b</xref>
</td>
<td align="left" valign="top" charoff="50">Heterotroph
Sulfate reducers</td>
<td align="left" valign="top" charoff="50"><italic>Desulfatiferula, Desulfobulbus, Desulfocapsa, Desulfosalsimonas</italic>
</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Syntrophobacterales
<italic>Deltaproteobacteria</italic>
</td>
<td align="left" valign="top" charoff="50">Arnon<xref ref-type="fn" rid="t3-fn2">a</xref>
Reductive acetyl-CoA(?)<xref ref-type="fn" rid="t3-fn3">b</xref>
</td>
<td align="left" valign="top" charoff="50">Heterotroph
Sulfate reducer/
sulfide oxidation
SRAO</td>
<td align="left" valign="top" charoff="50"><italic>Desulfomonile</italic>
</td>
</tr>
<tr><td align="left" valign="top" charoff="50">Desulfuromonadales
<italic>Deltaproteobacteria</italic>
</td>
<td align="left" valign="top" charoff="50">Reductive acetyl-CoA<xref ref-type="fn" rid="t3-fn3">b</xref>
</td>
<td align="left" valign="top" charoff="50">Nitrate dependent Fe(II) oxidation with production of ammonium (<xref ref-type="bibr" rid="bib59">Weber <italic>et al.,</italic>
2006</xref>
)</td>
<td align="left" valign="top" charoff="50"> </td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="t3-fn1"><p>Abbreviation: SRAO, sulfate-reducing ammonium oxidation.</p>
</fn>
<fn id="t3-fn2"><label>a</label>
<p>Also known as reverse Krebs cycle, reverse tricarboxylic acid cycle (rTCA) and reverse citric acid cycle.</p>
</fn>
<fn id="t3-fn3"><label>b</label>
<p>Also known as Wood–Ljungdahl pathway.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
</record>
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