Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes
Identifieur interne : 000330 ( Pmc/Checkpoint ); précédent : 000329; suivant : 000331Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes
Auteurs : Pascal Hingamp [France] ; Nigel Grimsley [France] ; Silvia G. Acinas [Espagne] ; Camille Clerissi [France] ; Lucie Subirana [France] ; Julie Poulain [France] ; Isabel Ferrera [Espagne] ; Hugo Sarmento [Espagne] ; Emilie Villar [France] ; Gipsi Lima-Mendez [Belgique] ; Karoline Faust [Belgique] ; Shinichi Sunagawa [Allemagne] ; Jean-Michel Claverie [France] ; Hervé Moreau [France] ; Yves Desdevises [France] ; Peer Bork [Allemagne] ; Jeroen Raes [Belgique] ; Colomban De Vargas [France] ; Eric Karsenti [Allemagne] ; Stefanie Kandels-Lewis [Allemagne] ; Olivier Jaillon [France] ; Fabrice Not [France] ; Stéphane Pesant [Allemagne] ; Patrick Wincker [France] ; Hiroyuki Ogata [France, Japon]Source :
- The ISME Journal [ 1751-7362 ] ; 2013.
Abstract
Nucleo-cytoplasmic large DNA viruses (NCLDVs) constitute a group of eukaryotic viruses that can have crucial ecological roles in the sea by accelerating the turnover of their unicellular hosts or by causing diseases in animals. To better characterize the diversity, abundance and biogeography of marine NCLDVs, we analyzed 17 metagenomes derived from microbial samples (0.2–1.6 μm size range) collected during the Tara Oceans Expedition. The sample set includes ecosystems under-represented in previous studies, such as the Arabian Sea oxygen minimum zone (OMZ) and Indian Ocean lagoons. By combining computationally derived relative abundance and direct prokaryote cell counts, the abundance of NCLDVs was found to be in the order of 104–105 genomes ml−1 for the samples from the photic zone and 102–103 genomes ml−1 for the OMZ. The Megaviridae and Phycodnaviridae dominated the NCLDV populations in the metagenomes, although most of the reads classified in these families showed large divergence from known viral genomes. Our taxon co-occurrence analysis revealed a potential association between viruses of the Megaviridae family and eukaryotes related to oomycetes. In support of this predicted association, we identified six cases of lateral gene transfer between Megaviridae and oomycetes. Our results suggest that marine NCLDVs probably outnumber eukaryotic organisms in the photic layer (per given water mass) and that metagenomic sequence analyses promise to shed new light on the biodiversity of marine viruses and their interactions with potential hosts.
Url:
DOI: 10.1038/ismej.2013.59
PubMed: 23575371
PubMed Central: 3749498
Affiliations:
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PMC:3749498Le document en format XML
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<author><name sortKey="Villar, Emilie" sort="Villar, Emilie" uniqKey="Villar E" first="Emilie" last="Villar">Emilie Villar</name>
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<author><name sortKey="Raes, Jeroen" sort="Raes, Jeroen" uniqKey="Raes J" first="Jeroen" last="Raes">Jeroen Raes</name>
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<author><name sortKey="Pesant, Stephane" sort="Pesant, Stephane" uniqKey="Pesant S" first="Stéphane" last="Pesant">Stéphane Pesant</name>
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, Bremen,<country>Germany</country>
</nlm:aff>
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<author><name sortKey="Wincker, Patrick" sort="Wincker, Patrick" uniqKey="Wincker P" first="Patrick" last="Wincker">Patrick Wincker</name>
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</nlm:aff>
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<author><name sortKey="Ogata, Hiroyuki" sort="Ogata, Hiroyuki" uniqKey="Ogata H" first="Hiroyuki" last="Ogata">Hiroyuki Ogata</name>
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, Marseille,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<affiliation wicri:level="1"><nlm:aff id="aff10"><institution>Education Academy of Computational Life Sciences, Tokyo Institute of Technology</institution>
, Tokyo,<country>Japan</country>
</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes</title>
<author><name sortKey="Hingamp, Pascal" sort="Hingamp, Pascal" uniqKey="Hingamp P" first="Pascal" last="Hingamp">Pascal Hingamp</name>
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, Marseille,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
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<author><name sortKey="Grimsley, Nigel" sort="Grimsley, Nigel" uniqKey="Grimsley N" first="Nigel" last="Grimsley">Nigel Grimsley</name>
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</nlm:aff>
<country xml:lang="fr">France</country>
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<author><name sortKey="Acinas, Silvia G" sort="Acinas, Silvia G" uniqKey="Acinas S" first="Silvia G" last="Acinas">Silvia G. Acinas</name>
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, Barcelona,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
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<author><name sortKey="Clerissi, Camille" sort="Clerissi, Camille" uniqKey="Clerissi C" first="Camille" last="Clerissi">Camille Clerissi</name>
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, Banyuls-sur-Mer,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Subirana, Lucie" sort="Subirana, Lucie" uniqKey="Subirana L" first="Lucie" last="Subirana">Lucie Subirana</name>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>CNRS and Université Pierre et Marie (Paris 06), UMR 7232, Observatoire Océanologique</institution>
, Banyuls-sur-Mer,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Poulain, Julie" sort="Poulain, Julie" uniqKey="Poulain J" first="Julie" last="Poulain">Julie Poulain</name>
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, Evry,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Ferrera, Isabel" sort="Ferrera, Isabel" uniqKey="Ferrera I" first="Isabel" last="Ferrera">Isabel Ferrera</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Marine Biology and Oceanography, Institute of Marine Science (ICM), CSIC, Passeig Marítim de la Barceloneta</institution>
, Barcelona,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
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<author><name sortKey="Sarmento, Hugo" sort="Sarmento, Hugo" uniqKey="Sarmento H" first="Hugo" last="Sarmento">Hugo Sarmento</name>
<affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Department of Marine Biology and Oceanography, Institute of Marine Science (ICM), CSIC, Passeig Marítim de la Barceloneta</institution>
, Barcelona,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Villar, Emilie" sort="Villar, Emilie" uniqKey="Villar E" first="Emilie" last="Villar">Emilie Villar</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>CNRS, Aix-Marseille Université, Laboratoire Information Génomique et Structurale (UMR 7256), Mediterranean Institute of Microbiology (FR 3479)</institution>
, Marseille,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
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<author><name sortKey="Lima Mendez, Gipsi" sort="Lima Mendez, Gipsi" uniqKey="Lima Mendez G" first="Gipsi" last="Lima-Mendez">Gipsi Lima-Mendez</name>
<affiliation wicri:level="1"><nlm:aff id="aff5"><institution>Department of Structural Biology, VIB</institution>
, Brussel,<country>Belgium</country>
</nlm:aff>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff6"><institution>Department of Applied Biological Sciences (DBIT), Vrije Universiteit Brussel</institution>
, Brussels,<country>Belgium</country>
</nlm:aff>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Faust, Karoline" sort="Faust, Karoline" uniqKey="Faust K" first="Karoline" last="Faust">Karoline Faust</name>
<affiliation wicri:level="1"><nlm:aff id="aff5"><institution>Department of Structural Biology, VIB</institution>
, Brussel,<country>Belgium</country>
</nlm:aff>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff6"><institution>Department of Applied Biological Sciences (DBIT), Vrije Universiteit Brussel</institution>
, Brussels,<country>Belgium</country>
</nlm:aff>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Sunagawa, Shinichi" sort="Sunagawa, Shinichi" uniqKey="Sunagawa S" first="Shinichi" last="Sunagawa">Shinichi Sunagawa</name>
<affiliation wicri:level="1"><nlm:aff id="aff7"><institution>European Molecular Biology Laboratory</institution>
, Heidelberg,<country>Germany</country>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Claverie, Jean Michel" sort="Claverie, Jean Michel" uniqKey="Claverie J" first="Jean-Michel" last="Claverie">Jean-Michel Claverie</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>CNRS, Aix-Marseille Université, Laboratoire Information Génomique et Structurale (UMR 7256), Mediterranean Institute of Microbiology (FR 3479)</institution>
, Marseille,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Moreau, Herve" sort="Moreau, Herve" uniqKey="Moreau H" first="Hervé" last="Moreau">Hervé Moreau</name>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>CNRS and Université Pierre et Marie (Paris 06), UMR 7232, Observatoire Océanologique</institution>
, Banyuls-sur-Mer,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Desdevises, Yves" sort="Desdevises, Yves" uniqKey="Desdevises Y" first="Yves" last="Desdevises">Yves Desdevises</name>
<affiliation wicri:level="1"><nlm:aff id="aff2"><institution>CNRS and Université Pierre et Marie (Paris 06), UMR 7232, Observatoire Océanologique</institution>
, Banyuls-sur-Mer,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Bork, Peer" sort="Bork, Peer" uniqKey="Bork P" first="Peer" last="Bork">Peer Bork</name>
<affiliation wicri:level="1"><nlm:aff id="aff7"><institution>European Molecular Biology Laboratory</institution>
, Heidelberg,<country>Germany</country>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Raes, Jeroen" sort="Raes, Jeroen" uniqKey="Raes J" first="Jeroen" last="Raes">Jeroen Raes</name>
<affiliation wicri:level="1"><nlm:aff id="aff5"><institution>Department of Structural Biology, VIB</institution>
, Brussel,<country>Belgium</country>
</nlm:aff>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff6"><institution>Department of Applied Biological Sciences (DBIT), Vrije Universiteit Brussel</institution>
, Brussels,<country>Belgium</country>
</nlm:aff>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="De Vargas, Colomban" sort="De Vargas, Colomban" uniqKey="De Vargas C" first="Colomban" last="De Vargas">Colomban De Vargas</name>
<affiliation wicri:level="1"><nlm:aff id="aff8"><institution>CNRS, Université Pierre et Marie Curie (Paris 06), UMR 7144, Station Biologique de Roscoff</institution>
, Roscoff,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Karsenti, Eric" sort="Karsenti, Eric" uniqKey="Karsenti E" first="Eric" last="Karsenti">Eric Karsenti</name>
<affiliation wicri:level="1"><nlm:aff id="aff7"><institution>European Molecular Biology Laboratory</institution>
, Heidelberg,<country>Germany</country>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Kandels Lewis, Stefanie" sort="Kandels Lewis, Stefanie" uniqKey="Kandels Lewis S" first="Stefanie" last="Kandels-Lewis">Stefanie Kandels-Lewis</name>
<affiliation wicri:level="1"><nlm:aff id="aff7"><institution>European Molecular Biology Laboratory</institution>
, Heidelberg,<country>Germany</country>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Jaillon, Olivier" sort="Jaillon, Olivier" uniqKey="Jaillon O" first="Olivier" last="Jaillon">Olivier Jaillon</name>
<affiliation wicri:level="1"><nlm:aff id="aff4"><institution>CEA, Institut de Génomique, Genoscope</institution>
, Evry,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Not, Fabrice" sort="Not, Fabrice" uniqKey="Not F" first="Fabrice" last="Not">Fabrice Not</name>
<affiliation wicri:level="1"><nlm:aff id="aff8"><institution>CNRS, Université Pierre et Marie Curie (Paris 06), UMR 7144, Station Biologique de Roscoff</institution>
, Roscoff,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Pesant, Stephane" sort="Pesant, Stephane" uniqKey="Pesant S" first="Stéphane" last="Pesant">Stéphane Pesant</name>
<affiliation wicri:level="1"><nlm:aff id="aff9"><institution>MARUM—Center for Marine Environmental Sciences, Universität Bremen</institution>
, Bremen,<country>Germany</country>
</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Wincker, Patrick" sort="Wincker, Patrick" uniqKey="Wincker P" first="Patrick" last="Wincker">Patrick Wincker</name>
<affiliation wicri:level="1"><nlm:aff id="aff4"><institution>CEA, Institut de Génomique, Genoscope</institution>
, Evry,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Ogata, Hiroyuki" sort="Ogata, Hiroyuki" uniqKey="Ogata H" first="Hiroyuki" last="Ogata">Hiroyuki Ogata</name>
<affiliation wicri:level="1"><nlm:aff id="aff1"><institution>CNRS, Aix-Marseille Université, Laboratoire Information Génomique et Structurale (UMR 7256), Mediterranean Institute of Microbiology (FR 3479)</institution>
, Marseille,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff10"><institution>Education Academy of Computational Life Sciences, Tokyo Institute of Technology</institution>
, Tokyo,<country>Japan</country>
</nlm:aff>
<country xml:lang="fr">Japon</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">The ISME Journal</title>
<idno type="ISSN">1751-7362</idno>
<idno type="eISSN">1751-7370</idno>
<imprint><date when="2013">2013</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><p>Nucleo-cytoplasmic large DNA viruses (NCLDVs) constitute a group of eukaryotic viruses that can have crucial ecological roles in the sea by accelerating the turnover of their unicellular hosts or by causing diseases in animals. To better characterize the diversity, abundance and biogeography of marine NCLDVs, we analyzed 17 metagenomes derived from microbial samples (0.2–1.6 μm size range) collected during the Tara Oceans Expedition. The sample set includes ecosystems under-represented in previous studies, such as the Arabian Sea oxygen minimum zone (OMZ) and Indian Ocean lagoons. By combining computationally derived relative abundance and direct prokaryote cell counts, the abundance of NCLDVs was found to be in the order of 10<sup>4</sup>
–10<sup>5</sup>
genomes ml<sup>−1</sup>
for the samples from the photic zone and 10<sup>2</sup>
–10<sup>3</sup>
genomes ml<sup>−1</sup>
for the OMZ. The Megaviridae and Phycodnaviridae dominated the NCLDV populations in the metagenomes, although most of the reads classified in these families showed large divergence from known viral genomes. Our taxon co-occurrence analysis revealed a potential association between viruses of the Megaviridae family and eukaryotes related to oomycetes. In support of this predicted association, we identified six cases of lateral gene transfer between Megaviridae and oomycetes. Our results suggest that marine NCLDVs probably outnumber eukaryotic organisms in the photic layer (per given water mass) and that metagenomic sequence analyses promise to shed new light on the biodiversity of marine viruses and their interactions with potential hosts.</p>
</div>
</front>
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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">23575371</article-id>
<article-id pub-id-type="pmc">3749498</article-id>
<article-id pub-id-type="pii">ismej201359</article-id>
<article-id pub-id-type="doi">10.1038/ismej.2013.59</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Original Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes</article-title>
<alt-title alt-title-type="running">NCLDVs in Tara Oceans metagenomes</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Hingamp</surname>
<given-names>Pascal</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="author-notes" rid="note1"><sup>11</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Grimsley</surname>
<given-names>Nigel</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Acinas</surname>
<given-names>Silvia G</given-names>
</name>
<xref ref-type="aff" rid="aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Clerissi</surname>
<given-names>Camille</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Subirana</surname>
<given-names>Lucie</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Poulain</surname>
<given-names>Julie</given-names>
</name>
<xref ref-type="aff" rid="aff4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ferrera</surname>
<given-names>Isabel</given-names>
</name>
<xref ref-type="aff" rid="aff3">3</xref>
<xref ref-type="author-notes" rid="note2"><sup>12</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sarmento</surname>
<given-names>Hugo</given-names>
</name>
<xref ref-type="aff" rid="aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Villar</surname>
<given-names>Emilie</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lima-Mendez</surname>
<given-names>Gipsi</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>Faust</surname>
<given-names>Karoline</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>Sunagawa</surname>
<given-names>Shinichi</given-names>
</name>
<xref ref-type="aff" rid="aff7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Claverie</surname>
<given-names>Jean-Michel</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Moreau</surname>
<given-names>Hervé</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Desdevises</surname>
<given-names>Yves</given-names>
</name>
<xref ref-type="aff" rid="aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bork</surname>
<given-names>Peer</given-names>
</name>
<xref ref-type="aff" rid="aff7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Raes</surname>
<given-names>Jeroen</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>de Vargas</surname>
<given-names>Colomban</given-names>
</name>
<xref ref-type="aff" rid="aff8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Karsenti</surname>
<given-names>Eric</given-names>
</name>
<xref ref-type="aff" rid="aff7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kandels-Lewis</surname>
<given-names>Stefanie</given-names>
</name>
<xref ref-type="aff" rid="aff7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jaillon</surname>
<given-names>Olivier</given-names>
</name>
<xref ref-type="aff" rid="aff4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Not</surname>
<given-names>Fabrice</given-names>
</name>
<xref ref-type="aff" rid="aff8">8</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pesant</surname>
<given-names>Stéphane</given-names>
</name>
<xref ref-type="aff" rid="aff9">9</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wincker</surname>
<given-names>Patrick</given-names>
</name>
<xref ref-type="aff" rid="aff4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ogata</surname>
<given-names>Hiroyuki</given-names>
</name>
<xref ref-type="aff" rid="aff1">1</xref>
<xref ref-type="aff" rid="aff10">10</xref>
<xref ref-type="author-notes" rid="note1"><sup>11</sup>
</xref>
<xref ref-type="corresp" rid="caf1">*</xref>
</contrib>
<aff id="aff1"><label>1</label>
<institution>CNRS, Aix-Marseille Université, Laboratoire Information Génomique et Structurale (UMR 7256), Mediterranean Institute of Microbiology (FR 3479)</institution>
, Marseille,<country>France</country>
</aff>
<aff id="aff2"><label>2</label>
<institution>CNRS and Université Pierre et Marie (Paris 06), UMR 7232, Observatoire Océanologique</institution>
, Banyuls-sur-Mer,<country>France</country>
</aff>
<aff id="aff3"><label>3</label>
<institution>Department of Marine Biology and Oceanography, Institute of Marine Science (ICM), CSIC, Passeig Marítim de la Barceloneta</institution>
, Barcelona,<country>Spain</country>
</aff>
<aff id="aff4"><label>4</label>
<institution>CEA, Institut de Génomique, Genoscope</institution>
, Evry,<country>France</country>
</aff>
<aff id="aff5"><label>5</label>
<institution>Department of Structural Biology, VIB</institution>
, Brussel,<country>Belgium</country>
</aff>
<aff id="aff6"><label>6</label>
<institution>Department of Applied Biological Sciences (DBIT), Vrije Universiteit Brussel</institution>
, Brussels,<country>Belgium</country>
</aff>
<aff id="aff7"><label>7</label>
<institution>European Molecular Biology Laboratory</institution>
, Heidelberg,<country>Germany</country>
</aff>
<aff id="aff8"><label>8</label>
<institution>CNRS, Université Pierre et Marie Curie (Paris 06), UMR 7144, Station Biologique de Roscoff</institution>
, Roscoff,<country>France</country>
</aff>
<aff id="aff9"><label>9</label>
<institution>MARUM—Center for Marine Environmental Sciences, Universität Bremen</institution>
, Bremen,<country>Germany</country>
</aff>
<aff id="aff10"><label>10</label>
<institution>Education Academy of Computational Life Sciences, Tokyo Institute of Technology</institution>
, Tokyo,<country>Japan</country>
</aff>
</contrib-group>
<author-notes><corresp id="caf1"><label>*</label>
<institution>Education Academy of Computational Life Sciences, Tokyo Institute of Technology, 2-12-1, Ookayama, Meguro-ku</institution>
, Tokyo 152 8552, <country>Japan</country>
. E-mail: <email>ogata@acls.titech.ac.jp</email>
, <email>hiroyuki.ogata@igs.cnrs-mrs.fr</email>
</corresp>
<fn fn-type="present-address" id="note1"><label>11</label>
<p>These authors contributed equally to this work.</p>
</fn>
<fn fn-type="present-address" id="note2"><label>12</label>
<p>Current address: Departament de Genètica i de Microbiologia, Universitat Autònoma de Barcelona, Bellaterra ES-08193, Spain.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><month>09</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="epub"><day>11</day>
<month>04</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>1</day>
<month>9</month>
<year>2013</year>
</pub-date>
<volume>7</volume>
<issue>9</issue>
<fpage>1678</fpage>
<lpage>1695</lpage>
<history><date date-type="received"><day>06</day>
<month>11</month>
<year>2012</year>
</date>
<date date-type="rev-recd"><day>28</day>
<month>02</month>
<year>2013</year>
</date>
<date date-type="accepted"><day>06</day>
<month>03</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2013 International Society for Microbial Ecology</copyright-statement>
<copyright-year>2013</copyright-year>
<copyright-holder>International Society for Microbial Ecology</copyright-holder>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/3.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 3.0 Unported License. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/3.0/">http://creativecommons.org/licenses/by/3.0/</ext-link>
</license-p>
</license>
</permissions>
<abstract><p>Nucleo-cytoplasmic large DNA viruses (NCLDVs) constitute a group of eukaryotic viruses that can have crucial ecological roles in the sea by accelerating the turnover of their unicellular hosts or by causing diseases in animals. To better characterize the diversity, abundance and biogeography of marine NCLDVs, we analyzed 17 metagenomes derived from microbial samples (0.2–1.6 μm size range) collected during the Tara Oceans Expedition. The sample set includes ecosystems under-represented in previous studies, such as the Arabian Sea oxygen minimum zone (OMZ) and Indian Ocean lagoons. By combining computationally derived relative abundance and direct prokaryote cell counts, the abundance of NCLDVs was found to be in the order of 10<sup>4</sup>
–10<sup>5</sup>
genomes ml<sup>−1</sup>
for the samples from the photic zone and 10<sup>2</sup>
–10<sup>3</sup>
genomes ml<sup>−1</sup>
for the OMZ. The Megaviridae and Phycodnaviridae dominated the NCLDV populations in the metagenomes, although most of the reads classified in these families showed large divergence from known viral genomes. Our taxon co-occurrence analysis revealed a potential association between viruses of the Megaviridae family and eukaryotes related to oomycetes. In support of this predicted association, we identified six cases of lateral gene transfer between Megaviridae and oomycetes. Our results suggest that marine NCLDVs probably outnumber eukaryotic organisms in the photic layer (per given water mass) and that metagenomic sequence analyses promise to shed new light on the biodiversity of marine viruses and their interactions with potential hosts.</p>
</abstract>
<kwd-group><kwd>eukaryotic viruses</kwd>
<kwd>marine NCLDVs</kwd>
<kwd>taxon co-occurrence</kwd>
<kwd>oomycetes</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="fig1"><label>Figure 1</label>
<caption><p>Metagenome-based relative abundance of NCLDV and cellular genomes in the TOP data set. Seventeen TOP metagenomes (0.2–1.6 μm size fraction) were pooled and analyzed as a single data set to generate this plot. Each dot in the plot represents the density of one of the marker genes used in this study (16 markers for NCLDVs and 35 markers for cellular genomes). The estimated abundance of NCLDVs genomes is slightly lower than that of Archaea genomes and amounts to approximately 3% of bacterial genomes.</p>
</caption>
<graphic xlink:href="ismej201359f1"></graphic>
</fig>
<fig id="fig2"><label>Figure 2</label>
<caption><p>NCLDV genome abundance in the TOP data set. (<bold>a</bold>
) Proportion of the average marker gene density for NCLDVs relative to that of prokaryotes (Bacteria and Archaea) for each of the 17 TOP metagenomes. (<bold>b</bold>
) Experimentally measured prokaryotic cell densities (gray circles; 16 samples by microscopy and 13 samples by FC) were used to estimate the absolute abundances of NCLDV genomes (black squares) by rescaling the metagenome-based relative abundances. ‘S', ‘D' and ‘Z' in the sample names indicate the depths from which the samples were collected: ‘S' for surface, ‘D' for deep chlorophyll max and ‘Z' for oxygen minimum zone.</p>
</caption>
<graphic xlink:href="ismej201359f2"></graphic>
</fig>
<fig id="fig3"><label>Figure 3</label>
<caption><p>Metagenome-based relative abundance of NCLDV families. (<bold>a</bold>
) Representation of different viral groups in the whole TOP metagenomic data set as measured by the NCLDV marker gene density. The number of marker reads taxonomically assigned to each viral group is shown in parentheses in the legend. (<bold>b</bold>
) Representation of different viral groups in the 17 TOP metagenomic samples. ‘S', ‘D' and ‘Z' in the sample names indicate the depths from which the samples were collected: ‘S' for surface, ‘D' for deep chlorophyll max and ‘Z' for oxygen minimum zone. In both (<bold>a</bold>
) and (<bold>b</bold>
), three reads and one read assigned to Asfarviridae and Poxviridae, respectively, were omitted for presentation purpose.</p>
</caption>
<graphic xlink:href="ismej201359f3"></graphic>
</fig>
<fig id="fig4"><label>Figure 4</label>
<caption><p>Phylogenetic positions of metagenomic reads closely related to NCLDV DNA polymerase sequences. An HMM search with a PolB profile detected 2028 PolB-like peptide sequences in the TOP metagenomes. Each of these peptides was placed within a large reference phylogenetic tree containing diverse viral and cellular homologs (<xref ref-type="supplementary-material" rid="sup1">Supplementary Figure S1</xref>
) with the use of Pplacer. Of these peptides, 264 were mapped on the branches leading to NCLDV sequences and are shown in this figure. The numbers of mapped metagenomic reads are shown on the branches and are reflected by branch widths. This result is consistent with the preponderance of the Phycodnaviridae and Megaviridae families seen in our BLAST-based marker gene analysis. Only the NCLDV part of the reference tree is shown.</p>
</caption>
<graphic xlink:href="ismej201359f4"></graphic>
</fig>
<fig id="fig5"><label>Figure 5</label>
<caption><p>Classification of NCLDV marker genes in the TOP data based on the level of sequence similarity to database sequences. Metagenomic reads showing ⩾80% amino-acid sequence identity to database sequences were classified as ‘known (or seen)', otherwise as ‘novel (or unseen)'. (<bold>a</bold>
) BLAST result against UniProt. (<bold>b</bold>
) BLAST result against the GOS data. The large proportions of ‘novel (and unseen)' genes suggest current environmental surveys are far from reaching saturation and that diverse yet unknown NCLDVs exist in the sea.</p>
</caption>
<graphic xlink:href="ismej201359f5"></graphic>
</fig>
<fig id="fig6"><label>Figure 6</label>
<caption><p>Taxon associations inferred from co-occurrence analysis. (<bold>a</bold>
) Distribution of <italic>P</italic>
-values for Spearman's correlation coefficients for taxon associations observed in the TOP metagenomic data. Colored (red and green) areas of the histogram represent taxon pairs showing statistically significant correlations. The position of the <italic>P</italic>
-value for the hypothetical positive association between the ‘Megaviridae' and ‘oomycetes' taxonomic groups is indicated by a red triangle. (<bold>b</bold>
) Correlated occurrence of 454 reads taxonomically assigned to the ‘Megaviridae' and the ‘oomycetes' groups by the BLAST-based 2bLCA method. Each dot corresponds to one of the 17 TOP samples analyzed. Axes represent the density of these reads (number of reads per Mbp) for each of the ‘Megaviridae' and the ‘oomycetes' groups.</p>
</caption>
<graphic xlink:href="ismej201359f6"></graphic>
</fig>
<fig id="fig7"><label>Figure 7</label>
<caption><p>Evidence of horizontal gene transfer between viruses and eukaryotes related to oomycetes. The displayed maximum likelihood tree was generated based on sequences of the Mimivirus hypothetical vWFA domain-containing protein (gi: 311978223) and its homologs using PhyML. The numbers on the branches indicate bootstrap percentages after 100 bootstrap sampling. The tree was mid-point rooted for visualization purpose. The grouping of the Megaviridae and oomycete sequences suggests a gene exchange between the lineage leading to Megaviridae and the lineage leading to oomycetes. Phylogenetic trees for the remaining five putative cases of horizontal gene transfers between these lineages are provided in the <xref ref-type="supplementary-material" rid="sup1">Supplementary Figure S9</xref>
.</p>
</caption>
<graphic xlink:href="ismej201359f7"></graphic>
</fig>
<table-wrap id="tbl1"><label>Table 1</label>
<caption><title>General description of the samples analyzed in this study</title>
</caption>
<table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col>
<col align="char" char="."></col>
<col align="left"></col>
<col align="left"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="center"></col>
<col align="char" char="."></col>
<col align="left"></col>
</colgroup>
<thead valign="bottom"><tr><th align="left" valign="top" charoff="50"><italic>Name</italic>
</th>
<th align="center" valign="top" char="." charoff="50"><italic>Station number</italic>
</th>
<th align="left" valign="top" charoff="50"><italic>Region</italic>
</th>
<th align="left" valign="top" charoff="50"><italic>Marine system type</italic>
</th>
<th align="center" valign="top" charoff="50"><italic>Depth (m)</italic>
</th>
<th align="center" valign="top" charoff="50"><italic>Location</italic>
<xref ref-type="fn" rid="t1-fn2">a</xref>
</th>
<th align="center" valign="top" charoff="50"><italic>T (°C)</italic>
</th>
<th align="center" valign="top" charoff="50"><italic>Salinity (psu)</italic>
</th>
<th align="center" valign="top" charoff="50"><italic>Chl a (mg Chl a m</italic>
<sup><italic>−3</italic>
</sup>
)</th>
<th align="center" valign="top" char="." charoff="50"><italic>Date and time (UTC)</italic>
<xref ref-type="fn" rid="t1-fn2">a</xref>
</th>
<th align="left" valign="top" charoff="50"><italic>Sample identifiers</italic>
</th>
</tr>
</thead>
<tbody valign="top"><tr><td align="left" valign="top" charoff="50">3_S</td>
<td align="char" valign="top" char="." charoff="50">3</td>
<td align="left" valign="top" charoff="50">Atlantic Ocean</td>
<td align="left" valign="top" charoff="50">Open ocean</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">36°43.520'N 10°28.250'W</td>
<td align="center" valign="top" charoff="50">NA</td>
<td align="center" valign="top" charoff="50">NA</td>
<td align="center" valign="top" charoff="50">NA</td>
<td align="char" valign="top" char="." charoff="50">2009/09/13 10:40</td>
<td align="left" valign="top" charoff="50">TARA-Y200000001 (A6.1)</td>
</tr>
<tr><td align="left" valign="top" charoff="50">4_S</td>
<td align="char" valign="top" char="." charoff="50">4</td>
<td align="left" valign="top" charoff="50">Atlantic Ocean</td>
<td align="left" valign="top" charoff="50">Open ocean</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">36°33.200'N 6°34.010'W</td>
<td align="center" valign="top" charoff="50">NA</td>
<td align="center" valign="top" charoff="50">NA</td>
<td align="center" valign="top" charoff="50">NA</td>
<td align="char" valign="top" char="." charoff="50">2009/09/15 10:15</td>
<td align="left" valign="top" charoff="50">TARA-Y200000002 (A11)</td>
</tr>
<tr><td align="left" valign="top" charoff="50">6_S</td>
<td align="char" valign="top" char="." charoff="50">6</td>
<td align="left" valign="top" charoff="50">Mediterranean Sea</td>
<td align="left" valign="top" charoff="50">Enclosed sea</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">36°31.239'N 4°0.443'W</td>
<td align="char" valign="top" char="." charoff="50">17.0</td>
<td align="char" valign="top" char="." charoff="50">37.35</td>
<td align="char" valign="top" char="." charoff="50">3.121</td>
<td align="char" valign="top" char="." charoff="50">2009/09/21 14:49</td>
<td align="left" valign="top" charoff="50">TARA-Y200000003 (A32)</td>
</tr>
<tr><td align="left" valign="top" charoff="50">7_S</td>
<td align="char" valign="top" char="." charoff="50">7</td>
<td align="left" valign="top" charoff="50">Mediterranean Sea</td>
<td align="left" valign="top" charoff="50">Enclosed sea</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">37°2.321'N 1°56.99'W</td>
<td align="char" valign="top" char="." charoff="50">23.8</td>
<td align="char" valign="top" char="." charoff="50">37.48</td>
<td align="char" valign="top" char="." charoff="50">0.075</td>
<td align="char" valign="top" char="." charoff="50">2009/09/23 17:05</td>
<td align="left" valign="top" charoff="50">TARA-A200000113</td>
</tr>
<tr><td align="left" valign="top" charoff="50">7_D</td>
<td align="char" valign="top" char="." charoff="50">7</td>
<td align="left" valign="top" charoff="50">Mediterranean Sea</td>
<td align="left" valign="top" charoff="50">Enclosed sea</td>
<td align="center" valign="top" charoff="50">DCM
(42 m)</td>
<td align="center" valign="top" charoff="50">37°2.321'N 1°56.99'W</td>
<td align="char" valign="top" char="." charoff="50">17.8</td>
<td align="char" valign="top" char="." charoff="50">37.09</td>
<td align="char" valign="top" char="." charoff="50">0.296</td>
<td align="char" valign="top" char="." charoff="50">2009/09/23 17:05</td>
<td align="left" valign="top" charoff="50">TARA-A200000159</td>
</tr>
<tr><td align="left" valign="top" charoff="50">23_S</td>
<td align="char" valign="top" char="." charoff="50">23</td>
<td align="left" valign="top" charoff="50">Mediterranean Sea</td>
<td align="left" valign="top" charoff="50">Enclosed sea</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">42°10.462'N 17°43.163'E</td>
<td align="char" valign="top" char="." charoff="50">17.1</td>
<td align="char" valign="top" char="." charoff="50">38.22</td>
<td align="char" valign="top" char="." charoff="50">0.036</td>
<td align="char" valign="top" char="." charoff="50">2009/11/18 12:44</td>
<td align="left" valign="top" charoff="50">TARA-E500000066</td>
</tr>
<tr><td align="left" valign="top" charoff="50">23_D</td>
<td align="char" valign="top" char="." charoff="50">23</td>
<td align="left" valign="top" charoff="50">Mediterranean Sea</td>
<td align="left" valign="top" charoff="50">Enclosed sea</td>
<td align="center" valign="top" charoff="50">DCM
(56 m)</td>
<td align="center" valign="top" charoff="50">42°10.462'N 17°43.163'E</td>
<td align="char" valign="top" char="." charoff="50">16.0</td>
<td align="char" valign="top" char="." charoff="50">38.30</td>
<td align="char" valign="top" char="." charoff="50">0.119</td>
<td align="char" valign="top" char="." charoff="50">2009/11/18 12:44</td>
<td align="left" valign="top" charoff="50">TARA-E500000081</td>
</tr>
<tr><td align="left" valign="top" charoff="50">30_S</td>
<td align="char" valign="top" char="." charoff="50">30</td>
<td align="left" valign="top" charoff="50">Mediterranean Sea</td>
<td align="left" valign="top" charoff="50">Enclosed sea</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">33°55.077'N 32°53.622'E</td>
<td align="char" valign="top" char="." charoff="50">20.4</td>
<td align="char" valign="top" char="." charoff="50">39.42</td>
<td align="char" valign="top" char="." charoff="50">0.025</td>
<td align="char" valign="top" char="." charoff="50">2009/12/14 12:44</td>
<td align="left" valign="top" charoff="50">TARA-A100001568</td>
</tr>
<tr><td align="left" valign="top" charoff="50">31_S</td>
<td align="char" valign="top" char="." charoff="50">31</td>
<td align="left" valign="top" charoff="50">Red Sea</td>
<td align="left" valign="top" charoff="50">Enclosed sea</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">27°8.100'N 34°48.400'E</td>
<td align="char" valign="top" char="." charoff="50">25.0</td>
<td align="char" valign="top" char="." charoff="50">39.91</td>
<td align="char" valign="top" char="." charoff="50">0.005</td>
<td align="char" valign="top" char="." charoff="50">2010/01/09 10:03</td>
<td align="left" valign="top" charoff="50">TARA-A100001568</td>
</tr>
<tr><td align="left" valign="top" charoff="50">36_S</td>
<td align="char" valign="top" char="." charoff="50">36</td>
<td align="left" valign="top" charoff="50">Arabian Sea</td>
<td align="left" valign="top" charoff="50">Semi-enclosed sea</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">20°49.053'N 63°30.727'E</td>
<td align="char" valign="top" char="." charoff="50">26.0</td>
<td align="char" valign="top" char="." charoff="50">36.53</td>
<td align="char" valign="top" char="." charoff="50">0.047</td>
<td align="char" valign="top" char="." charoff="50">2010/03/12 10:36</td>
<td align="left" valign="top" charoff="50">TARA-Y100000022</td>
</tr>
<tr><td align="left" valign="top" charoff="50">38_S</td>
<td align="char" valign="top" char="." charoff="50">38</td>
<td align="left" valign="top" charoff="50">Arabian Sea</td>
<td align="left" valign="top" charoff="50">Semi-enclosed sea</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">19°2.318'N 64°29.620'E</td>
<td align="char" valign="top" char="." charoff="50">26.3</td>
<td align="char" valign="top" char="." charoff="50">36.62</td>
<td align="char" valign="top" char="." charoff="50">0.052</td>
<td align="char" valign="top" char="." charoff="50">2010/03/15 03:45</td>
<td align="left" valign="top" charoff="50">TARA-Y100000288</td>
</tr>
<tr><td align="left" valign="top" charoff="50">38_Z</td>
<td align="char" valign="top" char="." charoff="50">38</td>
<td align="left" valign="top" charoff="50">Arabian Sea</td>
<td align="left" valign="top" charoff="50">Semi-enclosed sea</td>
<td align="center" valign="top" charoff="50">OMZ
(350 m)</td>
<td align="center" valign="top" charoff="50">19°2.103'N 64°33.825'E</td>
<td align="char" valign="top" char="." charoff="50">14.7</td>
<td align="char" valign="top" char="." charoff="50">36.00</td>
<td align="char" valign="top" char="." charoff="50">0.002</td>
<td align="char" valign="top" char="." charoff="50">2010/03/16 06:14</td>
<td align="left" valign="top" charoff="50">TARA-Y100000294</td>
</tr>
<tr><td align="left" valign="top" charoff="50">39_S</td>
<td align="char" valign="top" char="." charoff="50">39</td>
<td align="left" valign="top" charoff="50">Arabian Sea</td>
<td align="left" valign="top" charoff="50">Semi-enclosed sea</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">18°34.213'N 66°29.167'E</td>
<td align="char" valign="top" char="." charoff="50">27.4</td>
<td align="char" valign="top" char="." charoff="50">36.29</td>
<td align="char" valign="top" char="." charoff="50">0.026</td>
<td align="char" valign="top" char="." charoff="50">2010/03/18 09:56</td>
<td align="left" valign="top" charoff="50">TARA-Y100000029</td>
</tr>
<tr><td align="left" valign="top" charoff="50">39_Z</td>
<td align="char" valign="top" char="." charoff="50">39</td>
<td align="left" valign="top" charoff="50">Arabian Sea</td>
<td align="left" valign="top" charoff="50">Semi-enclosed sea</td>
<td align="center" valign="top" charoff="50">OMZ
(270 m)</td>
<td align="center" valign="top" charoff="50">18°44.043'N 66°23.375'E</td>
<td align="char" valign="top" char="." charoff="50">15.6</td>
<td align="char" valign="top" char="." charoff="50">35.91</td>
<td align="char" valign="top" char="." charoff="50">0.003</td>
<td align="char" valign="top" char="." charoff="50">2010/03/20 08:17</td>
<td align="left" valign="top" charoff="50">TARA-Y100000031</td>
</tr>
<tr><td align="left" valign="top" charoff="50">43_S</td>
<td align="char" valign="top" char="." charoff="50">43</td>
<td align="left" valign="top" charoff="50">Indian Ocean</td>
<td align="left" valign="top" charoff="50">Lagoon</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">4°39.582'N 73°29.128'E</td>
<td align="char" valign="top" char="." charoff="50">30.0</td>
<td align="char" valign="top" char="." charoff="50">34.49</td>
<td align="char" valign="top" char="." charoff="50">0.075</td>
<td align="char" valign="top" char="." charoff="50">2010/04/05 08:50</td>
<td align="left" valign="top" charoff="50">TARA-Y100000074</td>
</tr>
<tr><td align="left" valign="top" charoff="50">46_S</td>
<td align="char" valign="top" char="." charoff="50">46</td>
<td align="left" valign="top" charoff="50">Indian Ocean</td>
<td align="left" valign="top" charoff="50">Lagoon</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">0°39.748'S 73°9.664'E</td>
<td align="char" valign="top" char="." charoff="50">30.1</td>
<td align="char" valign="top" char="." charoff="50">35.11</td>
<td align="char" valign="top" char="." charoff="50">0.050</td>
<td align="char" valign="top" char="." charoff="50">2010/04/15 02:40</td>
<td align="left" valign="top" charoff="50">TARA-Y100000100</td>
</tr>
<tr><td align="left" valign="top" charoff="50">49_S</td>
<td align="char" valign="top" char="." charoff="50">49</td>
<td align="left" valign="top" charoff="50">Indian Ocean</td>
<td align="left" valign="top" charoff="50">Open ocean</td>
<td align="center" valign="top" charoff="50">SRF</td>
<td align="center" valign="top" charoff="50">16°48.497'S 59°30.257'E</td>
<td align="char" valign="top" char="." charoff="50">28.3</td>
<td align="char" valign="top" char="." charoff="50">34.49</td>
<td align="char" valign="top" char="." charoff="50">0.024</td>
<td align="char" valign="top" char="." charoff="50">2010/04/23 10:29</td>
<td align="left" valign="top" charoff="50">TARA-Y100000120</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="t1-fn1"><p>Abbreviations: DCM, deep chlorophyll maximum; NA, not applicable; OMZ, oxyzen minimum zone; SRF, surface; UTC, Coordinated Universal Time.</p>
</fn>
<fn id="t1-fn2"><label>a</label>
<p>Locations, date and time correspond to events for the collection of contextual physicochemical data. Events for water sampling could slightly differ from these values.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="tbl2"><label>Table 2</label>
<caption><title>Quality-controlled Tara Oceans pyrosequence data</title>
</caption>
<table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col>
<col align="char" char="."></col>
<col align="char" char="."></col>
<col align="char" char="."></col>
<col align="char" char="."></col>
<col align="char" char="."></col>
<col align="char" char="."></col>
</colgroup>
<thead valign="bottom"><tr><th align="left" valign="top" charoff="50"><italic>Sample name</italic>
</th>
<th align="center" valign="top" char="." charoff="50"><italic>Total size (bp)</italic>
</th>
<th align="center" valign="top" char="." charoff="50"><italic>Number of reads</italic>
</th>
<th align="center" valign="top" char="." charoff="50"><italic>G+C (%)</italic>
</th>
<th align="center" valign="top" char="." charoff="50"><italic>Average size (bp)</italic>
</th>
<th align="center" valign="top" char="." charoff="50"><italic>Number of predicted ORFs</italic>
</th>
<th align="center" valign="top" char="." charoff="50"><italic>Average ORF size (aa)</italic>
</th>
</tr>
</thead>
<tbody valign="top"><tr><td align="left" valign="top" charoff="50">3_S</td>
<td align="char" valign="top" char="." charoff="50">21 533 646</td>
<td align="char" valign="top" char="." charoff="50">63 994</td>
<td align="char" valign="top" char="." charoff="50">37</td>
<td align="char" valign="top" char="." charoff="50">336</td>
<td align="char" valign="top" char="." charoff="50">65 656</td>
<td align="char" valign="top" char="." charoff="50">99</td>
</tr>
<tr><td align="left" valign="top" charoff="50">4_S</td>
<td align="char" valign="top" char="." charoff="50">52 953 075</td>
<td align="char" valign="top" char="." charoff="50">140 754</td>
<td align="char" valign="top" char="." charoff="50">38</td>
<td align="char" valign="top" char="." charoff="50">376</td>
<td align="char" valign="top" char="." charoff="50">149 018</td>
<td align="char" valign="top" char="." charoff="50">108</td>
</tr>
<tr><td align="left" valign="top" charoff="50">6_S</td>
<td align="char" valign="top" char="." charoff="50">36 129 806</td>
<td align="char" valign="top" char="." charoff="50">95 255</td>
<td align="char" valign="top" char="." charoff="50">48</td>
<td align="char" valign="top" char="." charoff="50">379</td>
<td align="char" valign="top" char="." charoff="50">98 996</td>
<td align="char" valign="top" char="." charoff="50">111</td>
</tr>
<tr><td align="left" valign="top" charoff="50">7_S</td>
<td align="char" valign="top" char="." charoff="50">98 750 180</td>
<td align="char" valign="top" char="." charoff="50">332 049</td>
<td align="char" valign="top" char="." charoff="50">38</td>
<td align="char" valign="top" char="." charoff="50">297</td>
<td align="char" valign="top" char="." charoff="50">335 408</td>
<td align="char" valign="top" char="." charoff="50">90</td>
</tr>
<tr><td align="left" valign="top" charoff="50">7_D</td>
<td align="char" valign="top" char="." charoff="50">279 389 388</td>
<td align="char" valign="top" char="." charoff="50">1 117 888</td>
<td align="char" valign="top" char="." charoff="50">37</td>
<td align="char" valign="top" char="." charoff="50">250</td>
<td align="char" valign="top" char="." charoff="50">1 013 853</td>
<td align="char" valign="top" char="." charoff="50">81</td>
</tr>
<tr><td align="left" valign="top" charoff="50">23_S</td>
<td align="char" valign="top" char="." charoff="50">67 695 268</td>
<td align="char" valign="top" char="." charoff="50">196 190</td>
<td align="char" valign="top" char="." charoff="50">39</td>
<td align="char" valign="top" char="." charoff="50">345</td>
<td align="char" valign="top" char="." charoff="50">201 447</td>
<td align="char" valign="top" char="." charoff="50">101</td>
</tr>
<tr><td align="left" valign="top" charoff="50">23_D</td>
<td align="char" valign="top" char="." charoff="50">83 539 478</td>
<td align="char" valign="top" char="." charoff="50">239 447</td>
<td align="char" valign="top" char="." charoff="50">38</td>
<td align="char" valign="top" char="." charoff="50">349</td>
<td align="char" valign="top" char="." charoff="50">246 948</td>
<td align="char" valign="top" char="." charoff="50">102</td>
</tr>
<tr><td align="left" valign="top" charoff="50">30_S</td>
<td align="char" valign="top" char="." charoff="50">89 180 466</td>
<td align="char" valign="top" char="." charoff="50">256 028</td>
<td align="char" valign="top" char="." charoff="50">37</td>
<td align="char" valign="top" char="." charoff="50">348</td>
<td align="char" valign="top" char="." charoff="50">268 616</td>
<td align="char" valign="top" char="." charoff="50">101</td>
</tr>
<tr><td align="left" valign="top" charoff="50">31_S</td>
<td align="char" valign="top" char="." charoff="50">245 463 121</td>
<td align="char" valign="top" char="." charoff="50">614 743</td>
<td align="char" valign="top" char="." charoff="50">39</td>
<td align="char" valign="top" char="." charoff="50">399</td>
<td align="char" valign="top" char="." charoff="50">660 949</td>
<td align="char" valign="top" char="." charoff="50">114</td>
</tr>
<tr><td align="left" valign="top" charoff="50">36_S</td>
<td align="char" valign="top" char="." charoff="50">245 945 064</td>
<td align="char" valign="top" char="." charoff="50">737 506</td>
<td align="char" valign="top" char="." charoff="50">39</td>
<td align="char" valign="top" char="." charoff="50">333</td>
<td align="char" valign="top" char="." charoff="50">757 448</td>
<td align="char" valign="top" char="." charoff="50">100</td>
</tr>
<tr><td align="left" valign="top" charoff="50">38_S</td>
<td align="char" valign="top" char="." charoff="50">214 253 370</td>
<td align="char" valign="top" char="." charoff="50">601 110</td>
<td align="char" valign="top" char="." charoff="50">39</td>
<td align="char" valign="top" char="." charoff="50">356</td>
<td align="char" valign="top" char="." charoff="50">631 351</td>
<td align="char" valign="top" char="." charoff="50">103</td>
</tr>
<tr><td align="left" valign="top" charoff="50">38_Z</td>
<td align="char" valign="top" char="." charoff="50">223 188 575</td>
<td align="char" valign="top" char="." charoff="50">638 843</td>
<td align="char" valign="top" char="." charoff="50">45</td>
<td align="char" valign="top" char="." charoff="50">349</td>
<td align="char" valign="top" char="." charoff="50">659 041</td>
<td align="char" valign="top" char="." charoff="50">104</td>
</tr>
<tr><td align="left" valign="top" charoff="50">39_S</td>
<td align="char" valign="top" char="." charoff="50">233 273 851</td>
<td align="char" valign="top" char="." charoff="50">590 664</td>
<td align="char" valign="top" char="." charoff="50">43</td>
<td align="char" valign="top" char="." charoff="50">395</td>
<td align="char" valign="top" char="." charoff="50">629 501</td>
<td align="char" valign="top" char="." charoff="50">114</td>
</tr>
<tr><td align="left" valign="top" charoff="50">39_Z</td>
<td align="char" valign="top" char="." charoff="50">249 558 778</td>
<td align="char" valign="top" char="." charoff="50">679 589</td>
<td align="char" valign="top" char="." charoff="50">46</td>
<td align="char" valign="top" char="." charoff="50">367</td>
<td align="char" valign="top" char="." charoff="50">708 056</td>
<td align="char" valign="top" char="." charoff="50">108</td>
</tr>
<tr><td align="left" valign="top" charoff="50">43_S</td>
<td align="char" valign="top" char="." charoff="50">167 515 516</td>
<td align="char" valign="top" char="." charoff="50">529 506</td>
<td align="char" valign="top" char="." charoff="50">37</td>
<td align="char" valign="top" char="." charoff="50">316</td>
<td align="char" valign="top" char="." charoff="50">545 641</td>
<td align="char" valign="top" char="." charoff="50">93</td>
</tr>
<tr><td align="left" valign="top" charoff="50">46_S</td>
<td align="char" valign="top" char="." charoff="50">251 310 870</td>
<td align="char" valign="top" char="." charoff="50">648 425</td>
<td align="char" valign="top" char="." charoff="50">41</td>
<td align="char" valign="top" char="." charoff="50">388</td>
<td align="char" valign="top" char="." charoff="50">689 641</td>
<td align="char" valign="top" char="." charoff="50">112</td>
</tr>
<tr><td align="left" valign="top" charoff="50">49_S</td>
<td align="char" valign="top" char="." charoff="50">222 417 021</td>
<td align="char" valign="top" char="." charoff="50">680 573</td>
<td align="char" valign="top" char="." charoff="50">43</td>
<td align="char" valign="top" char="." charoff="50">327</td>
<td align="char" valign="top" char="." charoff="50">696 974</td>
<td align="char" valign="top" char="." charoff="50">98</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="t2-fn1"><p>Abbreviation: ORF, open reading frame.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="tbl3"><label>Table 3</label>
<caption><title>Examples of positive and negative viral-cell associations</title>
</caption>
<table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col>
<col align="left"></col>
<col align="char" char="."></col>
<col align="left"></col>
<col align="center"></col>
<col align="center"></col>
</colgroup>
<thead valign="bottom"><tr><th align="left" valign="top" charoff="50"><italic>Taxon 1</italic>
</th>
<th align="left" valign="top" charoff="50"><italic>Taxon 2</italic>
</th>
<th align="center" valign="top" char="." charoff="50"><italic>ρ</italic>
</th>
<th align="left" valign="top" charoff="50"><italic>q</italic>
</th>
<th align="center" valign="top" charoff="50"><italic>ρ</italic>
'</th>
<th align="center" valign="top" charoff="50"><italic>q</italic>
'</th>
</tr>
</thead>
<tbody valign="top"><tr><td colspan="6" align="left" valign="top" charoff="50"><italic>Co-occurrence</italic>
</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Mimiviridae</td>
<td align="left" valign="top" charoff="50">Eukaryota; stramenopiles; Oomycetes</td>
<td align="char" valign="top" char="." charoff="50">0.949</td>
<td align="center" valign="top" charoff="50">2.22E-05</td>
<td align="char" valign="top" char="." charoff="50">0.939</td>
<td align="center" valign="top" charoff="50">1.7E-02</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Iridoviridae; Lymphocystivirus; unclassified Lymphocystivirus</td>
<td align="left" valign="top" charoff="50">Bacteria; Tenericutes; Mollicutes; Mycoplasmataceae</td>
<td align="char" valign="top" char="." charoff="50">0.883</td>
<td align="center" valign="top" charoff="50">1.44E-03</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; unclassified phages; environmental samples</td>
<td align="left" valign="top" charoff="50">Bacteria; Cyanobacteria; environmental samples</td>
<td align="char" valign="top" char="." charoff="50">0.864</td>
<td align="center" valign="top" charoff="50">2.92E-03</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Caudovirales; Siphoviridae</td>
<td align="left" valign="top" charoff="50">Eukaryota; Alveolata; Apicomplexa; Aconoidasida; Piroplasmida</td>
<td align="char" valign="top" char="." charoff="50">0.861</td>
<td align="center" valign="top" charoff="50">3.26E-03</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Herpesvirales; Herpesviridae; Gammaherpesvirinae</td>
<td align="left" valign="top" charoff="50">Bacteria; Proteobacteria; Gammaproteobacteria; Thiotrichales; Thiotrichaceae</td>
<td align="char" valign="top" char="." charoff="50">0.853</td>
<td align="center" valign="top" charoff="50">4.20E-03</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Phycodnaviridae</td>
<td align="left" valign="top" charoff="50">Bacteria; Proteobacteria; Gammaproteobacteria; Alteromonadales; Alteromonadales genera incertae sedis</td>
<td align="char" valign="top" char="." charoff="50">0.838</td>
<td align="center" valign="top" charoff="50">6.30E-03</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsRNA viruses; Reoviridae; Sedoreovirinae; Mimoreovirus</td>
<td align="left" valign="top" charoff="50">Eukaryota; Metazoa; Chordata; Craniata</td>
<td align="char" valign="top" char="." charoff="50">0.834</td>
<td align="center" valign="top" charoff="50">6.98E-03</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Herpesvirales; Herpesviridae; Gammaherpesvirinae</td>
<td align="left" valign="top" charoff="50">Bacteria; Chloroflexi; Thermomicrobiales; Thermomicrobiaceae; Thermomicrobium</td>
<td align="char" valign="top" char="." charoff="50">0.830</td>
<td align="center" valign="top" charoff="50">7.61E-03</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Herpesvirales; Herpesviridae; Gammaherpesvirinae</td>
<td align="left" valign="top" charoff="50">Bacteria; Proteobacteria; Magnetococcus</td>
<td align="char" valign="top" char="." charoff="50">0.825</td>
<td align="center" valign="top" charoff="50">8.53E-03</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Phycodnaviridae; unclassified Phycodnaviridae</td>
<td align="left" valign="top" charoff="50">Eukaryota; Viridiplantae; Chlorophyta; Prasinophyceae; Mamiellales</td>
<td align="char" valign="top" char="." charoff="50">0.821</td>
<td align="center" valign="top" charoff="50">9.36E-03</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Herpesvirales; Herpesviridae; Gammaherpesvirinae</td>
<td align="left" valign="top" charoff="50">Bacteria; Acidobacteria; Solibacteres; Solibacterales; Solibacteraceae</td>
<td align="char" valign="top" char="." charoff="50">0.820</td>
<td align="center" valign="top" charoff="50">9.51E-03</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Herpesvirales; Herpesviridae; Gammaherpesvirinae</td>
<td align="left" valign="top" charoff="50">Bacteria; Proteobacteria; Deltaproteobacteria; Desulfobacterales; Desulfobacteraceae</td>
<td align="char" valign="top" char="." charoff="50">0.820</td>
<td align="center" valign="top" charoff="50">9.51E-03</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Caudovirales; Myoviridae; T4-like viruses</td>
<td align="left" valign="top" charoff="50">Bacteria; Cyanobacteria; environmental samples</td>
<td align="char" valign="top" char="." charoff="50">0.819</td>
<td align="center" valign="top" charoff="50">9.71E-03</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Caudovirales; Podoviridae; Autographivirinae</td>
<td align="left" valign="top" charoff="50">Bacteria; Cyanobacteria; environmental samples</td>
<td align="char" valign="top" char="." charoff="50">0.817</td>
<td align="center" valign="top" charoff="50">1.02E-02</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage</td>
<td align="left" valign="top" charoff="50">Eukaryota; Alveolata; Ciliophora; Intramacronucleata; Spirotrichea</td>
<td align="char" valign="top" char="." charoff="50">0.803</td>
<td align="center" valign="top" charoff="50">1.36E-02</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Caudovirales; Podoviridae; N4-like viruses</td>
<td align="left" valign="top" charoff="50">Bacteria; Firmicutes; Clostridia; Clostridiales; Peptococcaceae</td>
<td align="char" valign="top" char="." charoff="50">0.802</td>
<td align="center" valign="top" charoff="50">1.38E-02</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Caudovirales</td>
<td align="left" valign="top" charoff="50">Eukaryota; Alveolata; Apicomplexa; Aconoidasida; Piroplasmida</td>
<td align="char" valign="top" char="." charoff="50">0.802</td>
<td align="center" valign="top" charoff="50">1.39E-02</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Viruses; dsDNA viruses, no RNA stage; unclassified dsDNA viruses</td>
<td align="left" valign="top" charoff="50">Bacteria; Proteobacteria; Alphaproteobacteria; Rickettsiales; SAR11 cluster</td>
<td align="char" valign="top" char="." charoff="50">0.801</td>
<td align="center" valign="top" charoff="50">1.39E-02</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Phycodnaviridae; Phaeovirus</td>
<td align="left" valign="top" charoff="50">Eukaryota; stramenopiles; Actinophryidae; Actinophrys</td>
<td align="char" valign="top" char="." charoff="50">0.801</td>
<td align="center" valign="top" charoff="50">1.39E-02</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Phycodnaviridae; unclassified Phycodnaviridae</td>
<td align="left" valign="top" charoff="50">Eukaryota; Viridiplantae; Chlorophyta; Prasinophyceae; environmental samples</td>
<td align="char" valign="top" char="." charoff="50">0.800</td>
<td align="center" valign="top" charoff="50">1.42E-02</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
</tr>
<tr><td colspan="6" align="left" valign="top" charoff="50"><italic>Mutual exclusion</italic>
</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Caudovirales; Myoviridae; phiKZ-like viruses</td>
<td align="left" valign="top" charoff="50">Eukaryota; Euglenozoa; Kinetoplastida; Trypanosomatidae; Leishmania</td>
<td align="char" valign="top" char="." charoff="50">−0.742</td>
<td align="left" valign="top" charoff="50">3.32E-02</td>
<td align="char" valign="top" char="." charoff="50">—0.804</td>
<td align="center" valign="top" charoff="50">1.72E-02</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Iridoviridae; Ranavirus</td>
<td align="left" valign="top" charoff="50">Bacteria; candidate division OP8; environmental samples</td>
<td align="char" valign="top" char="." charoff="50">−0.751</td>
<td align="left" valign="top" charoff="50">2.95E-02</td>
<td align="char" valign="top" char="." charoff="50">−0.695</td>
<td align="center" valign="top" charoff="50">3.83E-02</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Caudovirales; Myoviridae; phiKZ-like viruses</td>
<td align="left" valign="top" charoff="50">Eukaryota; Rhodophyta; Bangiophyceae; Cyanidiales; Cyanidiaceae</td>
<td align="center" valign="top" char="." charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="char" valign="top" char="." charoff="50">−0.659</td>
<td align="center" valign="top" charoff="50">2.95E-02</td>
</tr>
<tr><td align="left" valign="top" charoff="50"> Viruses; dsDNA viruses, no RNA stage; Caudovirales; Myoviridae; phiKZ-like viruses</td>
<td align="left" valign="top" charoff="50">Bacteria; Spirochaetes; Spirochaetales; Spirochaetaceae</td>
<td align="center" valign="top" char="." charoff="50">—</td>
<td align="center" valign="top" charoff="50">—</td>
<td align="char" valign="top" char="." charoff="50">−0.715</td>
<td align="center" valign="top" charoff="50">3.95E-02</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn id="t3-fn1"><p>Abbreviation: dsDNA, double-stranded DNA.</p>
</fn>
<fn id="t3-fn2"><p>Statistical significance of taxon associations was assessed by two methods. <italic>ρ</italic>
(Spearman's correlation coefficient) and <italic>q</italic>
(false discovery rate) were calculated by the first method and <italic>ρ</italic>
' (Spearman's correlation coefficient) and <italic>q</italic>
' (false discovery rate) were calculated by a more stringent second method. See Materials and methods for details.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
<affiliations><list><country><li>Allemagne</li>
<li>Belgique</li>
<li>Espagne</li>
<li>France</li>
<li>Japon</li>
</country>
</list>
<tree><country name="France"><noRegion><name sortKey="Hingamp, Pascal" sort="Hingamp, Pascal" uniqKey="Hingamp P" first="Pascal" last="Hingamp">Pascal Hingamp</name>
</noRegion>
<name sortKey="Claverie, Jean Michel" sort="Claverie, Jean Michel" uniqKey="Claverie J" first="Jean-Michel" last="Claverie">Jean-Michel Claverie</name>
<name sortKey="Clerissi, Camille" sort="Clerissi, Camille" uniqKey="Clerissi C" first="Camille" last="Clerissi">Camille Clerissi</name>
<name sortKey="De Vargas, Colomban" sort="De Vargas, Colomban" uniqKey="De Vargas C" first="Colomban" last="De Vargas">Colomban De Vargas</name>
<name sortKey="Desdevises, Yves" sort="Desdevises, Yves" uniqKey="Desdevises Y" first="Yves" last="Desdevises">Yves Desdevises</name>
<name sortKey="Grimsley, Nigel" sort="Grimsley, Nigel" uniqKey="Grimsley N" first="Nigel" last="Grimsley">Nigel Grimsley</name>
<name sortKey="Jaillon, Olivier" sort="Jaillon, Olivier" uniqKey="Jaillon O" first="Olivier" last="Jaillon">Olivier Jaillon</name>
<name sortKey="Moreau, Herve" sort="Moreau, Herve" uniqKey="Moreau H" first="Hervé" last="Moreau">Hervé Moreau</name>
<name sortKey="Not, Fabrice" sort="Not, Fabrice" uniqKey="Not F" first="Fabrice" last="Not">Fabrice Not</name>
<name sortKey="Ogata, Hiroyuki" sort="Ogata, Hiroyuki" uniqKey="Ogata H" first="Hiroyuki" last="Ogata">Hiroyuki Ogata</name>
<name sortKey="Poulain, Julie" sort="Poulain, Julie" uniqKey="Poulain J" first="Julie" last="Poulain">Julie Poulain</name>
<name sortKey="Subirana, Lucie" sort="Subirana, Lucie" uniqKey="Subirana L" first="Lucie" last="Subirana">Lucie Subirana</name>
<name sortKey="Villar, Emilie" sort="Villar, Emilie" uniqKey="Villar E" first="Emilie" last="Villar">Emilie Villar</name>
<name sortKey="Wincker, Patrick" sort="Wincker, Patrick" uniqKey="Wincker P" first="Patrick" last="Wincker">Patrick Wincker</name>
</country>
<country name="Espagne"><noRegion><name sortKey="Acinas, Silvia G" sort="Acinas, Silvia G" uniqKey="Acinas S" first="Silvia G" last="Acinas">Silvia G. Acinas</name>
</noRegion>
<name sortKey="Ferrera, Isabel" sort="Ferrera, Isabel" uniqKey="Ferrera I" first="Isabel" last="Ferrera">Isabel Ferrera</name>
<name sortKey="Sarmento, Hugo" sort="Sarmento, Hugo" uniqKey="Sarmento H" first="Hugo" last="Sarmento">Hugo Sarmento</name>
</country>
<country name="Belgique"><noRegion><name sortKey="Lima Mendez, Gipsi" sort="Lima Mendez, Gipsi" uniqKey="Lima Mendez G" first="Gipsi" last="Lima-Mendez">Gipsi Lima-Mendez</name>
</noRegion>
<name sortKey="Faust, Karoline" sort="Faust, Karoline" uniqKey="Faust K" first="Karoline" last="Faust">Karoline Faust</name>
<name sortKey="Faust, Karoline" sort="Faust, Karoline" uniqKey="Faust K" first="Karoline" last="Faust">Karoline Faust</name>
<name sortKey="Lima Mendez, Gipsi" sort="Lima Mendez, Gipsi" uniqKey="Lima Mendez G" first="Gipsi" last="Lima-Mendez">Gipsi Lima-Mendez</name>
<name sortKey="Raes, Jeroen" sort="Raes, Jeroen" uniqKey="Raes J" first="Jeroen" last="Raes">Jeroen Raes</name>
<name sortKey="Raes, Jeroen" sort="Raes, Jeroen" uniqKey="Raes J" first="Jeroen" last="Raes">Jeroen Raes</name>
</country>
<country name="Allemagne"><noRegion><name sortKey="Sunagawa, Shinichi" sort="Sunagawa, Shinichi" uniqKey="Sunagawa S" first="Shinichi" last="Sunagawa">Shinichi Sunagawa</name>
</noRegion>
<name sortKey="Bork, Peer" sort="Bork, Peer" uniqKey="Bork P" first="Peer" last="Bork">Peer Bork</name>
<name sortKey="Kandels Lewis, Stefanie" sort="Kandels Lewis, Stefanie" uniqKey="Kandels Lewis S" first="Stefanie" last="Kandels-Lewis">Stefanie Kandels-Lewis</name>
<name sortKey="Karsenti, Eric" sort="Karsenti, Eric" uniqKey="Karsenti E" first="Eric" last="Karsenti">Eric Karsenti</name>
<name sortKey="Pesant, Stephane" sort="Pesant, Stephane" uniqKey="Pesant S" first="Stéphane" last="Pesant">Stéphane Pesant</name>
</country>
<country name="Japon"><noRegion><name sortKey="Ogata, Hiroyuki" sort="Ogata, Hiroyuki" uniqKey="Ogata H" first="Hiroyuki" last="Ogata">Hiroyuki Ogata</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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