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Nature. 2016 Sep 29;537(7622):689-693. doi: 10.1038/nature19366. Epub 2016 Sep 21.

Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses.

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Department of Microbiology, The Ohio State University, Columbus, Ohio 43210, USA.
Theoretical Biology and Bioinformatics, Utrecht University, 3584 CH Utrecht, The Netherlands.
Centre for Molecular and Biomolecular Informatics, Radboud University Medical Centre, 6525 GA Nijmegen, The Netherlands.
Department of Marine Biology, Federal University of Rio de Janeiro, Rio de Janeiro, CEP 21941-902, Brazil.
Structural and Computational Biology, European Molecular Biology Laboratory, 69117 Heidelberg, Germany.
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109, USA.
Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, Research Network Chemistry Meets Microbiology, University of Vienna, A-1090 Vienna, Austria.
Austrian Polar Research Institute, A-1090 Vienna, Austria.
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, USA.
Department of Marine Biology and Oceanography, Institut de Ciències del Mar (ICM), CSIC Barcelona E0800, Spain.
Institute of Marine Sciences (CNR-ISMAR), National Research Council, 30122 Venezia, Italy.
CEA - Institut de Génomique, GENOSCOPE, 91057 Evry, France.
PANGAEA, Data Publisher for Earth and Environmental Science, University of Bremen, 28359 Bremen, Germany.
MARUM, Bremen University, 28359 Bremen, Germany.
Directors' Research, European Molecular Biology Laboratory, 69117 Heidelberg, Germany.
CNRS, UMR 7144, EPEP, Station Biologique de Roscoff, 29680 Roscoff, France.
Sorbonne Universités, UPMC Université Paris 06, UMR 7144, Station Biologique de Roscoff, 29680 Roscoff, France.
Institut de Biologie de l'École Normale Supérieure, École Normale Supérieure, Paris Sciences et Lettres Research University, CNRS UMR 8197, INSERM U1024, F-75005 Paris, France.
CNRS, UMR 7093, Laboratoire d'océanographie de Villefranche, Observatoire Océanologique, 06230 Villefranche-sur-mer, France.
Sorbonne Universités, UPMC Université Paris 06, UMR 7093, Observatoire Océanologique, 06230 Villefranche-sur-mer, France.
Mediterranean Institute of Advanced Studies, CSIC-UiB, 21-07190 Esporles, Mallorca, Spain.
King Abdullah University of Science and Technology, Red Sea Research Center, Thuwal 23955-6900, Saudi Arabia.
Max-Delbrück-Centre for Molecular Medicine, 13092 Berlin, Germany.
CNRS, UMR 8030, 91057 Evry, France.
Université d'Evry, UMR 8030, 91057 Evry, France.
Department of Civil, Environmental and Geodetic Engineering, The Ohio State University, Columbus, Ohio 43210, USA.


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 '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.

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