Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses

Simon Roux, Jennifer R Brum, Bas E. Dutilh, Shinichi Sunagawa, Melissa B Duhaime, Alexander Loy, Bonnie T Poulos, Natalie Solonenko, Elena Lara, Julie Poulain, Stephane Pesant, Stefanie Kandels-Lewis, Celine Dimier, Marc Picheral, Sarah Searson, Corinne Cruaud, Adriana Alberti, Carlos M. Duarte, Josep M M Gasol, Dolors VaquePeer Bork, Silvia G Acinas, Patrick Wincker, Matthew B Sullivan

Research output: Contribution to journalArticlepeer-review

514 Scopus citations

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.
Original languageEnglish (US)
Pages (from-to)689-693
Number of pages5
JournalNature
Volume537
Issue number7622
DOIs
StatePublished - May 12 2016

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: 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.

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