Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses

Handle URI:
http://hdl.handle.net/10754/622394
Title:
Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses
Authors:
Roux, Simon; Brum, Jennifer R.; Dutilh, Bas E.; Sunagawa, Shinichi; Duhaime, Melissa B.; Loy, Alexander; Poulos, Bonnie T.; Solonenko, Natalie; Lara, Elena; Poulain, Julie; Pesant, Stéphane; Kandels-Lewis, Stefanie; Dimier, Céline; Picheral, Marc; Searson, Sarah; Cruaud, Corinne; Alberti, Adriana; Duarte, Carlos M. ( 0000-0002-1213-1361 ) ; Gasol, Josep M.; Vaqué, Dolors; Bork, Peer; Acinas, Silvia G.; Wincker, Patrick; Sullivan, Matthew B.
Abstract:
Ocean microbes drive biogeochemical cycling on a global scale. However, this cycling is constrained by viruses that affect community composition, metabolic activity, and evolutionary trajectories. Owing to challenges with the sampling and cultivation of viruses, genome-level viral diversity remains poorly described and grossly understudied, with less than 1% of observed surface-ocean viruses known. Here we assemble complete genomes and large genomic fragments from both surface-and deep-ocean viruses sampled during the Tara Oceans and Malaspina research expeditions, and analyse the resulting â global ocean virome' dataset to present a global map of abundant, double-stranded DNA viruses complete with genomic and ecological contexts. A total of 15,222 epipelagic and mesopelagic viral populations were identified, comprising 867 viral clusters (defined as approximately genus-level groups). This roughly triples the number of known ocean viral populations and doubles the number of candidate bacterial and archaeal virus genera, providing a near-complete sampling of epipelagic communities at both the population and viral-cluster level. We found that 38 of the 867 viral clusters were locally or globally abundant, together accounting for nearly half of the viral populations in any global ocean virome sample. While two-thirds of these clusters represent newly described viruses lacking any cultivated representative, most could be computationally linked to dominant, ecologically relevant microbial hosts. Moreover, we identified 243 viral-encoded auxiliary metabolic genes, of which only 95 were previously known. Deeper analyses of four of these auxiliary metabolic genes (dsrC, soxYZ, P-II (also known as glnB) and amoC) revealed that abundant viruses may directly manipulate sulfur and nitrogen cycling throughout the epipelagic ocean. This viral catalog and functional analyses provide a necessary foundation for the meaningful integration of viruses into ecosystem models where they act as key players in nutrient cycling and trophic networks. © 2016 Macmillan Publishers Limited, part of Springer Nature.
KAUST Department:
Red Sea Research Center (RSRC)
Citation:
Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB, et al. (2016) Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537: 689–693. Available: http://dx.doi.org/10.1038/nature19366.
Publisher:
Springer Nature
Journal:
Nature
Issue Date:
20-Sep-2016
DOI:
10.1038/nature19366
Type:
Article
ISSN:
0028-0836; 1476-4687
Sponsors:
We thank J. Weitz for advice on statistics, C. Pelikan for help with the DsrAB phylogenetic tree, C. Dahl for discussion regarding DsrC function, and members of the Sullivan and the V. Rich laboratories for suggestions and comments on this manuscript. We acknowledge support from UA high-performance computing and the Ohio Supercomputer Center. Sponsors and support for Tara Oceans and Malaspina expeditions are listed in the Supplementary Information. This viral research was funded by a National Science Foundation grant (1536989) and Gordon and Betty Moore Foundation grants (3790, 2631) to M.B.S., and the French Ministry of Research and Government through the ‘Investissements d’Avenir’ program OCEANOMICS (ANR-11-BTBR-0008) and France Genomique (ANR-10-INBS-09-08). Virus researchers were partially supported by the Water, Environmental and Energy Solutions Initiative and the Ecosystem Genomics Institute (S.R.), the Netherlands Organization for Scientific Research Vidi grant 864.14.004 and CAPES/BRASIL (B.E.D.), and the Austrian Science Fund (project P25111-B22, A.L.). Sequencing was provided by Genoscope (Tara Oceans) and DOE JGI (Malaspina). All authors approved the final manuscript. This article is contribution number 43 of the Tara Oceans expedition.
Additional Links:
http://www.nature.com/nature/journal/v537/n7622/full/nature19366.html
Appears in Collections:
Articles; Red Sea Research Center (RSRC)

Full metadata record

DC FieldValue Language
dc.contributor.authorRoux, Simonen
dc.contributor.authorBrum, Jennifer R.en
dc.contributor.authorDutilh, Bas E.en
dc.contributor.authorSunagawa, Shinichien
dc.contributor.authorDuhaime, Melissa B.en
dc.contributor.authorLoy, Alexanderen
dc.contributor.authorPoulos, Bonnie T.en
dc.contributor.authorSolonenko, Natalieen
dc.contributor.authorLara, Elenaen
dc.contributor.authorPoulain, Julieen
dc.contributor.authorPesant, Stéphaneen
dc.contributor.authorKandels-Lewis, Stefanieen
dc.contributor.authorDimier, Célineen
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.en
dc.contributor.authorVaqué, Dolorsen
dc.contributor.authorBork, Peeren
dc.contributor.authorAcinas, Silvia G.en
dc.contributor.authorWincker, Patricken
dc.contributor.authorSullivan, Matthew B.en
dc.date.accessioned2017-01-02T09:28:28Z-
dc.date.available2017-01-02T09:28:28Z-
dc.date.issued2016-09-20en
dc.identifier.citationRoux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB, et al. (2016) Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537: 689–693. Available: http://dx.doi.org/10.1038/nature19366.en
dc.identifier.issn0028-0836en
dc.identifier.issn1476-4687en
dc.identifier.doi10.1038/nature19366en
dc.identifier.urihttp://hdl.handle.net/10754/622394-
dc.description.abstractOcean microbes drive biogeochemical cycling on a global scale. However, this cycling is constrained by viruses that affect community composition, metabolic activity, and evolutionary trajectories. Owing to challenges with the sampling and cultivation of viruses, genome-level viral diversity remains poorly described and grossly understudied, with less than 1% of observed surface-ocean viruses known. Here we assemble complete genomes and large genomic fragments from both surface-and deep-ocean viruses sampled during the Tara Oceans and Malaspina research expeditions, and analyse the resulting â global ocean virome' dataset to present a global map of abundant, double-stranded DNA viruses complete with genomic and ecological contexts. A total of 15,222 epipelagic and mesopelagic viral populations were identified, comprising 867 viral clusters (defined as approximately genus-level groups). This roughly triples the number of known ocean viral populations and doubles the number of candidate bacterial and archaeal virus genera, providing a near-complete sampling of epipelagic communities at both the population and viral-cluster level. We found that 38 of the 867 viral clusters were locally or globally abundant, together accounting for nearly half of the viral populations in any global ocean virome sample. While two-thirds of these clusters represent newly described viruses lacking any cultivated representative, most could be computationally linked to dominant, ecologically relevant microbial hosts. Moreover, we identified 243 viral-encoded auxiliary metabolic genes, of which only 95 were previously known. Deeper analyses of four of these auxiliary metabolic genes (dsrC, soxYZ, P-II (also known as glnB) and amoC) revealed that abundant viruses may directly manipulate sulfur and nitrogen cycling throughout the epipelagic ocean. This viral catalog and functional analyses provide a necessary foundation for the meaningful integration of viruses into ecosystem models where they act as key players in nutrient cycling and trophic networks. © 2016 Macmillan Publishers Limited, part of Springer Nature.en
dc.description.sponsorshipWe thank J. Weitz for advice on statistics, C. Pelikan for help with the DsrAB phylogenetic tree, C. Dahl for discussion regarding DsrC function, and members of the Sullivan and the V. Rich laboratories for suggestions and comments on this manuscript. We acknowledge support from UA high-performance computing and the Ohio Supercomputer Center. Sponsors and support for Tara Oceans and Malaspina expeditions are listed in the Supplementary Information. This viral research was funded by a National Science Foundation grant (1536989) and Gordon and Betty Moore Foundation grants (3790, 2631) to M.B.S., and the French Ministry of Research and Government through the ‘Investissements d’Avenir’ program OCEANOMICS (ANR-11-BTBR-0008) and France Genomique (ANR-10-INBS-09-08). Virus researchers were partially supported by the Water, Environmental and Energy Solutions Initiative and the Ecosystem Genomics Institute (S.R.), the Netherlands Organization for Scientific Research Vidi grant 864.14.004 and CAPES/BRASIL (B.E.D.), and the Austrian Science Fund (project P25111-B22, A.L.). Sequencing was provided by Genoscope (Tara Oceans) and DOE JGI (Malaspina). All authors approved the final manuscript. This article is contribution number 43 of the Tara Oceans expedition.en
dc.publisherSpringer Natureen
dc.relation.urlhttp://www.nature.com/nature/journal/v537/n7622/full/nature19366.htmlen
dc.titleEcogenomics and potential biogeochemical impacts of globally abundant ocean virusesen
dc.typeArticleen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalNatureen
dc.contributor.institutionDepartment of Microbiology, Ohio State University, Columbus, OH, United Statesen
dc.contributor.institutionTheoretical Biology and Bioinformatics, Utrecht University, Utrecht, Netherlandsen
dc.contributor.institutionCentre for Molecular and Biomolecular Informatics, Radboud University Medical Centre, Nijmegen, 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 Biology, Institute of Microbiology, ETH Zurich, Zurich, Switzerlanden
dc.contributor.institutionDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, United Statesen
dc.contributor.institutionDivision of Microbial Ecology, Department of Microbiology and Ecosystem Science, Research Network Chemistry Meets Microbiology, Vienna, Austriaen
dc.contributor.institutionAustrian Polar Research Institute, Vienna, Austriaen
dc.contributor.institutionDepartment of Ecology and Evolutionary Biology, University of Arizona, Tucson, AR, United Statesen
dc.contributor.institutionDepartment of Marine Biology and Oceanography, Institut de Ciencies Del Mar, CSIC, Barcelona, Spainen
dc.contributor.institutionInstitute of Marine Sciences, National Research Council, Venezia, Italyen
dc.contributor.institutionPANGAEA, Data Publisher for Earth and Environmental Science, University of Bremen, Bremen, Germanyen
dc.contributor.institutionMARUM, Bremen University, Bremen, Germanyen
dc.contributor.institutionDepartment of Research European Molecular Biology Laboratory, Heidelberg, Germanyen
dc.contributor.institutionCNRS, Station Biologique de Roscoff, Roscoff, Franceen
dc.contributor.institutionSorbonne Universite.s, UPMC Universite, Roscoff, Franceen
dc.contributor.institutionInstitut de Biologie de LfEcole Normale Superieure, Ecole Normale Superieure, Paris Sciences et Lettres Research University, Paris, Franceen
dc.contributor.institutionCNRS, Laboratoire d'Oceanographie de Villefranche, Observatoire Oceanologique, Villefranche-sur-mer, Franceen
dc.contributor.institutionSorbonne Universites, UPMC Universite, Villefranche-sur-mer, Franceen
dc.contributor.institutionCEA, Institut de Genomique, Evry, Franceen
dc.contributor.institutionMediterranean Institute of Advanced Studies, CSIC, Esporles, Mallorca, Spainen
dc.contributor.institutionMax-Delbru.ck-Centre for Molecular Medicine, Berlin, Germanyen
dc.contributor.institutionCNRS, Evry, Franceen
dc.contributor.institutionUniversite DfEvry, Evry, Franceen
dc.contributor.institutionDepartment of Civil, Environmental and Geodetic Engineering, Ohio State University, Columbus, OH, United Statesen
kaust.authorDuarte, Carlos M.en
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