Exploring nucleo-cytoplasmic large DNA viruses in Tara Oceans microbial metagenomes
Identifieur interne : 000402 ( Ncbi/Checkpoint ); précédent : 000401; suivant : 000403Exploring 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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<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>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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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>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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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>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Clerissi, Camille" sort="Clerissi, Camille" uniqKey="Clerissi C" first="Camille" last="Clerissi">Camille Clerissi</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="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>
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<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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