Ecogenomics and biogeochemical impacts of uncultivated globally abundant ocean viruses

Handle URI:
http://hdl.handle.net/10754/619775
Title:
Ecogenomics and biogeochemical impacts of uncultivated globally abundant ocean viruses
Authors:
Roux, Simon; Brum, Jennifer R; Dutilh, Bas E. ( 0000-0003-2329-7890 ) ; Sunagawa, Shinichi ( 0000-0003-3065-0314 ) ; Duhaime, Melissa B ( 0000-0001-7884-5087 ) ; Loy, Alexander ( 0000-0001-8923-5882 ) ; Poulos, Bonnie T; Solonenko, Natalie; Lara, Elena ( 0000-0002-4625-348X ) ; Poulain, Julie; Pesant, Stephane ( 0000-0002-4936-5209 ) ; Kandels-Lewis, Stefanie ( 0000-0002-4194-4927 ) ; Dimier, Celine; Picheral, Marc; Searson, Sarah; Cruaud, Corinne; Alberti, Adriana; Duarte, Carlos M. ( 0000-0002-1213-1361 ) ; Gasol, Josep M M ( 0000-0001-5238-2387 ) ; Vaque, Dolors; Bork, Peer ( 0000-0002-2627-833X ) ; Acinas, Silvia G ( 0000-0002-3439-0428 ) ; Wincker, Patrick; Sullivan, Matthew B
Abstract:
Ocean microbes drive global-scale biogeochemical cycling, but do so under constraints imposed by viruses on host community composition, metabolism, and evolutionary trajectories. Due to sampling and cultivation challenges, genome-level viral diversity remains poorly described and grossly understudied in nature such that <1% of observed surface ocean viruses, even those that are abundant and ubiquitous, are ?known?. Here we analyze a global map of abundant, double stranded DNA (dsDNA) viruses and viral-encoded auxiliary metabolic genes (AMGs) with genomic and ecological contexts through the Global Ocean Viromes (GOV) dataset, which includes complete genomes and large genomic fragments from both surface and deep ocean viruses sampled during the Tara Oceans and Malaspina research expeditions. A total of 15,222 epi- and mesopelagic viral populations were identified that comprised 867 viral clusters (VCs, approximately genus-level groups). This roughly triples known ocean viral populations, doubles known candidate bacterial and archaeal virus genera, and near-completely samples epipelagic communities at both the population and VC level. Thirty-eight of the 867 VCs were identified as the most impactful dsDNA viral groups in the oceans, as these were locally or globally abundant and accounted together for nearly half of the viral populations in any GOV sample. Most of these were predicted in silico to infect dominant, ecologically relevant microbes, while two thirds of them represent newly described viruses that lacked any cultivated representative. Beyond these taxon-specific ecological observations, we identified 243 viral-encoded AMGs in GOV, only 95 of which were known. Deeper analyses of 4 of these AMGs revealed that abundant viruses directly manipulate sulfur and nitrogen cycling, and do so throughout the epipelagic ocean. Together these data provide a critically-needed organismal catalog and functional context to begin meaningfully integrating viruses into ecosystem models as key players in nutrient cycling and trophic networks.
KAUST Department:
Red Sea Research Center (RSRC)
Publisher:
Cold Spring Harbor Laboratory Press
Issue Date:
12-May-2016
DOI:
10.1101/053090
Type:
Article
Sponsors:
We thank Joshua Weitz for advice on statistics, Claus Pelikan for help with the DsrAB phylogenetic tree, Christiane Dahl for valuable discussion regarding DsrC function, and members of the Sullivan and Rich labs for suggestions and comments on this manuscript. We acknowledge support from UA highperformance computing and the Ohio Supercomputer Center. This viral research was funded by a National Science Foundation grant (#1536989) and Gordon and Betty Moore Foundation grants (#3790, #GBMF2631) to MBS. SR was partially supported by the University of Arizona Technology and Research Initiative Fund through the Water, Environmental and Energy Solutions Initiative and the Ecosystem Genomics Institute. BED was supported by the Netherlands Organization for Scientific Research (NWO) Vidi grant 864.14.004 and CAPES/BRASIL. AL was supported by the Austrian Science Fund (FWF, project P25111-B22). We thank all people who prepared virus samples on board: Silvia G Acinas, Defne Arslan, Lucie Bittner, Julia Boras, Encarna Borruell, Christophe Boutte, Camille Clerissi, Montserrat Coll, Francisco M. Cornejo-Castillo, Cristina D?ez Vives, Celine Dimier, Melissa Beth Duhaime, Isabel Ferrera, Laurence Garczarek, Nigel Grimsley, Pascal Hingamp, Lee Karp-Boss, Elena Lara, Noan LeBescot, Thomas Lefort, Hiroyuki Ogata, Eric Pelletier, Julie Poulain, Frank Prejger, Guillem Salazar, Lucie Subirana, Anne Thompson, Dolors Vaqu?, Emilie Villar, as well as Montse Sala for organizing the transfer and shipping of Malaspina samples. The Tara Oceans consortium effort was possible thanks to the commitment of the following people and sponsors: CNRS (in particular Groupement de Recherche GDR3280), European Molecular Biology Laboratory (EMBL), Genoscope/CEA, VIB, Stazione Zoologica Anton Dohrn, UNIMIB, Fund for Scientific Research ? Flanders, Rega Institute, KU Leuven, The French Ministry of Research, the French Government 'Investissements d'Avenir' programmes OCEANOMICS (ANR-11-BTBR-0008), FRANCE GENOMIQUE (ANR-10-INBS-09-08), MEMO LIFE (ANR-10-LABX-54), PSL* Research University (ANR-11-IDEX-0001-02), ANR (projects POSEIDON/ANR-09-BLAN-0348, PROMETHEUS/ANR-09-PCS-GENM-217, TARA-GIRUS/ANR-09-PCS-GENM-218), European Union FP7 (MicroB3/No.287589), ERC Advanced Grant Award to CB (Diatomite: 294823), BIO5, and Biosphere 2 to MBS, Spanish Ministry of Science and Innovation grant CGL2011-26848/BOS and MicroOcean PANGENOMICS to SGA, TANIT (CONES 2010-0036) from the Ag?ncia de Gesti? d ?Ajuts Universitaris i Recerca to SGA, JSPS KAKENHI Grant Number 26430184 to HO. We also thank the support and commitment of Agn?s b. and Etienne Bourgois, the Veolia Environment Foundation, Region Bretagne, Lorient Agglomeration, World Courier, Illumina, the EDF Foundation, FRB, the Prince Albert II de Monaco Foundation, the Tara schooner and its captains and crew. We thank MERCATOR-CORIOLIS and ACRI-ST for providing daily satellite data during the expedition. We are also grateful to the French Ministry of Foreign Affairs for supporting the expedition and to the countries who graciously granted sampling permissions. Tara Oceans would not exist without continuous support from 23 institutes (http://oceans.taraexpeditions.org). We also acknowledge excellent assistance from the European Bioinformatics Institute (EBI), as well as Yan Yuan and the EMBL IT core facility. Malaspina Expedition and Malaspinomics Projects are funded by the Spanish Ministry of Economy and Competitiveness (refs. CSD2008-00077 and CTM2011-15461-E) to CMD. Sequencing of the Malaspina viruses metagenomes was done at the Joint Genome Institute and was supported by US Department of Energy Joint Genome Institute 2011 Microbes Program grant CSP 602 to SGA. The work conducted by the US Department of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02?05CH11231. The authors further declare that all data reported herein are fully and freely available from the date of publication, with no restrictions, and that all of the samples, analyses, publications, and ownership of data are free from legal entanglement or restriction of any sort by the various nations whose waters the Tara Oceans expedition sampled in. Data described herein is available at EBI and PANGAEA (see Supplementary Table 1). All authors approved the final manuscript. This article is contribution number XXX of the Tara Oceans Expedition.
Additional Links:
http://biorxiv.org/content/early/2016/05/12/053090
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Full metadata record

DC FieldValue Language
dc.contributor.authorRoux, Simonen
dc.contributor.authorBrum, Jennifer Ren
dc.contributor.authorDutilh, Bas E.en
dc.contributor.authorSunagawa, Shinichien
dc.contributor.authorDuhaime, Melissa Ben
dc.contributor.authorLoy, Alexanderen
dc.contributor.authorPoulos, Bonnie Ten
dc.contributor.authorSolonenko, Natalieen
dc.contributor.authorLara, Elenaen
dc.contributor.authorPoulain, Julieen
dc.contributor.authorPesant, Stephaneen
dc.contributor.authorKandels-Lewis, Stefanieen
dc.contributor.authorDimier, Celineen
dc.contributor.authorPicheral, Marcen
dc.contributor.authorSearson, Sarahen
dc.contributor.authorCruaud, Corinneen
dc.contributor.authorAlberti, Adrianaen
dc.contributor.authorDuarte, Carlos M.en
dc.contributor.authorGasol, Josep M Men
dc.contributor.authorVaque, Dolorsen
dc.contributor.authorBork, Peeren
dc.contributor.authorAcinas, Silvia Gen
dc.contributor.authorWincker, Patricken
dc.contributor.authorSullivan, Matthew Ben
dc.date.accessioned2016-09-04T11:03:59Z-
dc.date.available2016-09-04T11:03:59Z-
dc.date.issued2016-05-12-
dc.identifier.doi10.1101/053090-
dc.identifier.urihttp://hdl.handle.net/10754/619775-
dc.description.abstractOcean microbes drive global-scale biogeochemical cycling, but do so under constraints imposed by viruses on host community composition, metabolism, and evolutionary trajectories. Due to sampling and cultivation challenges, genome-level viral diversity remains poorly described and grossly understudied in nature such that <1% of observed surface ocean viruses, even those that are abundant and ubiquitous, are ?known?. Here we analyze a global map of abundant, double stranded DNA (dsDNA) viruses and viral-encoded auxiliary metabolic genes (AMGs) with genomic and ecological contexts through the Global Ocean Viromes (GOV) dataset, which includes complete genomes and large genomic fragments from both surface and deep ocean viruses sampled during the Tara Oceans and Malaspina research expeditions. A total of 15,222 epi- and mesopelagic viral populations were identified that comprised 867 viral clusters (VCs, approximately genus-level groups). This roughly triples known ocean viral populations, doubles known candidate bacterial and archaeal virus genera, and near-completely samples epipelagic communities at both the population and VC level. Thirty-eight of the 867 VCs were identified as the most impactful dsDNA viral groups in the oceans, as these were locally or globally abundant and accounted together for nearly half of the viral populations in any GOV sample. Most of these were predicted in silico to infect dominant, ecologically relevant microbes, while two thirds of them represent newly described viruses that lacked any cultivated representative. Beyond these taxon-specific ecological observations, we identified 243 viral-encoded AMGs in GOV, only 95 of which were known. Deeper analyses of 4 of these AMGs revealed that abundant viruses directly manipulate sulfur and nitrogen cycling, and do so throughout the epipelagic ocean. Together these data provide a critically-needed organismal catalog and functional context to begin meaningfully integrating viruses into ecosystem models as key players in nutrient cycling and trophic networks.en
dc.description.sponsorshipWe thank Joshua Weitz for advice on statistics, Claus Pelikan for help with the DsrAB phylogenetic tree, Christiane Dahl for valuable discussion regarding DsrC function, and members of the Sullivan and Rich labs for suggestions and comments on this manuscript. We acknowledge support from UA highperformance computing and the Ohio Supercomputer Center. This viral research was funded by a National Science Foundation grant (#1536989) and Gordon and Betty Moore Foundation grants (#3790, #GBMF2631) to MBS. SR was partially supported by the University of Arizona Technology and Research Initiative Fund through the Water, Environmental and Energy Solutions Initiative and the Ecosystem Genomics Institute. BED was supported by the Netherlands Organization for Scientific Research (NWO) Vidi grant 864.14.004 and CAPES/BRASIL. AL was supported by the Austrian Science Fund (FWF, project P25111-B22). We thank all people who prepared virus samples on board: Silvia G Acinas, Defne Arslan, Lucie Bittner, Julia Boras, Encarna Borruell, Christophe Boutte, Camille Clerissi, Montserrat Coll, Francisco M. Cornejo-Castillo, Cristina D?ez Vives, Celine Dimier, Melissa Beth Duhaime, Isabel Ferrera, Laurence Garczarek, Nigel Grimsley, Pascal Hingamp, Lee Karp-Boss, Elena Lara, Noan LeBescot, Thomas Lefort, Hiroyuki Ogata, Eric Pelletier, Julie Poulain, Frank Prejger, Guillem Salazar, Lucie Subirana, Anne Thompson, Dolors Vaqu?, Emilie Villar, as well as Montse Sala for organizing the transfer and shipping of Malaspina samples. The Tara Oceans consortium effort was possible thanks to the commitment of the following people and sponsors: CNRS (in particular Groupement de Recherche GDR3280), European Molecular Biology Laboratory (EMBL), Genoscope/CEA, VIB, Stazione Zoologica Anton Dohrn, UNIMIB, Fund for Scientific Research ? Flanders, Rega Institute, KU Leuven, The French Ministry of Research, the French Government 'Investissements d'Avenir' programmes OCEANOMICS (ANR-11-BTBR-0008), FRANCE GENOMIQUE (ANR-10-INBS-09-08), MEMO LIFE (ANR-10-LABX-54), PSL* Research University (ANR-11-IDEX-0001-02), ANR (projects POSEIDON/ANR-09-BLAN-0348, PROMETHEUS/ANR-09-PCS-GENM-217, TARA-GIRUS/ANR-09-PCS-GENM-218), European Union FP7 (MicroB3/No.287589), ERC Advanced Grant Award to CB (Diatomite: 294823), BIO5, and Biosphere 2 to MBS, Spanish Ministry of Science and Innovation grant CGL2011-26848/BOS and MicroOcean PANGENOMICS to SGA, TANIT (CONES 2010-0036) from the Ag?ncia de Gesti? d ?Ajuts Universitaris i Recerca to SGA, JSPS KAKENHI Grant Number 26430184 to HO. We also thank the support and commitment of Agn?s b. and Etienne Bourgois, the Veolia Environment Foundation, Region Bretagne, Lorient Agglomeration, World Courier, Illumina, the EDF Foundation, FRB, the Prince Albert II de Monaco Foundation, the Tara schooner and its captains and crew. We thank MERCATOR-CORIOLIS and ACRI-ST for providing daily satellite data during the expedition. We are also grateful to the French Ministry of Foreign Affairs for supporting the expedition and to the countries who graciously granted sampling permissions. Tara Oceans would not exist without continuous support from 23 institutes (http://oceans.taraexpeditions.org). We also acknowledge excellent assistance from the European Bioinformatics Institute (EBI), as well as Yan Yuan and the EMBL IT core facility. Malaspina Expedition and Malaspinomics Projects are funded by the Spanish Ministry of Economy and Competitiveness (refs. CSD2008-00077 and CTM2011-15461-E) to CMD. Sequencing of the Malaspina viruses metagenomes was done at the Joint Genome Institute and was supported by US Department of Energy Joint Genome Institute 2011 Microbes Program grant CSP 602 to SGA. The work conducted by the US Department of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02?05CH11231. The authors further declare that all data reported herein are fully and freely available from the date of publication, with no restrictions, and that all of the samples, analyses, publications, and ownership of data are free from legal entanglement or restriction of any sort by the various nations whose waters the Tara Oceans expedition sampled in. Data described herein is available at EBI and PANGAEA (see Supplementary Table 1). All authors approved the final manuscript. This article is contribution number XXX of the Tara Oceans Expedition.en
dc.language.isoenen
dc.publisherCold Spring Harbor Laboratory Pressen
dc.relation.urlhttp://biorxiv.org/content/early/2016/05/12/053090en
dc.rightsThe copyright holder for this preprint is the author/funder. It is made available under a CC-BY-NC-ND 4.0 International license. http://creativecommons.org/licenses/by-nc-nd/4.0/en
dc.titleEcogenomics and biogeochemical impacts of uncultivated globally abundant ocean virusesen
dc.typeArticleen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.eprint.versionPre-printen
dc.contributor.institutionDepartment of Microbiology, The Ohio State University, Columbus, OH, USAen
dc.contributor.institutionTheoretical Biology and Bioinformatics, Utrecht University, Utrecht, The Netherlandsen
dc.contributor.institutionCentre for Molecular and Biomolecular Informatics, Radboud University Medical Centre, Nijmegen, The Netherlandsen
dc.contributor.institutionDepartment of Marine Biology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazilen
dc.contributor.institutionStructural and Computational Biology, European Molecular Biology Laboratory, Heidelberg, Germanyen
dc.contributor.institutionDepartment of Ecology and Evolutionary Biology, University of Michigan, MI, USAen
dc.contributor.institutionDivision of Microbial Ecology, Department of Microbiology and Ecosystem Science, Research Network Chemistry Meets Microbiology, University of Vienna, Vienna, Austriaen
dc.contributor.institutionAustrian Polar Research Institute, Vienna, Austriaen
dc.contributor.institutionDepartment of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, USAen
dc.contributor.institutionDepartment of Marine Biology and Oceanography, Institut de Ciencies del Mar (CSIC), Barcelona, Spainen
dc.contributor.institutionInstitute of Marine Sciences (CNR-ISMAR), National Research Council, Venezia, Italyen
dc.contributor.institutionCEA - Institut de Genomique, GENOSCOPE, Evry, Franceen
dc.contributor.institutionPANGAEA, Data Publisher for Earth and Environmental Science, University of Bremen, Bremen, Germanyen
dc.contributor.institutionMARUM, Bremen University, Bremen, Germanyen
dc.contributor.institutionDirectors' Research European Molecular Biology Laboratory, Heidelberg, Germanyen
dc.contributor.institutionSorbonne Universites, UPMC Universite Paris 06, CNRS, Laboratoire Adaptation et Diversite en Milieu Marin, Station Biologique de Roscoff, Roscoff, Franceen
dc.contributor.institutionSorbonne Universites, UPMC Universite Paris 06, CNRS, Laboratoire d?oceanographie de Villefranche (LOV), Observatoire Oceanologique, Villefranche-sur-Mer, Franceen
dc.contributor.institutionDepartment of Oceanography, University of Hawaii, Honolulu, Hawaii, USAen
dc.contributor.institutionMediterranean Institute of Advanced Studies, CSIC-UiB, Esporles, Mallorca, Spainen
dc.contributor.institutionMax-Delbruck-Centre for Molecular Medicine, 13092 Berlin, Germanyen
dc.contributor.institutionCNRS, UMR 8030, CP5706, Evry, Franceen
dc.contributor.institutionUniversite d'Evry, UMR 8030, CP5706, Evry, Franceen
dc.contributor.institutionDepartment of Civil, Environmental and Geodetic Engineering, The Ohio State University, Columbus, OH, USAen
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorDuarte, Carlos M.en
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