Marine DNA Viral Macro- and Microdiversity from Pole to Pole

Abstract
Microbes drive most ecosystems and are modulated by viruses that impact their lifespan, gene flow, and metabolic outputs. However, ecosystem-level impacts of viral community diversity remain difficult to assess due to classification issues and few reference genomes. Here, we establish an ∼12-fold expanded global ocean DNA virome dataset of 195,728 viral populations, now including the Arctic Ocean, and validate that these populations form discrete genotypic clusters. Meta-community analyses revealed five ecological zones throughout the global ocean, including two distinct Arctic regions. Across the zones, local and global patterns and drivers in viral community diversity were established for both macrodiversity (inter-population diversity) and microdiversity (intra-population genetic variation). These patterns sometimes, but not always, paralleled those from macro-organisms and revealed temperate and tropical surface waters and the Arctic as biodiversity hotspots and mechanistic hypotheses to explain them. Such further understanding of ocean viruses is critical for broader inclusion in ecosystem models. A global survey of ocean virus genomes vastly expands our understanding of this understudied community and reveals the Arctic as unexpected hotspot for viral biodiversity.

Citation
Gregory, A. C., Zayed, A. A., Conceição-Neto, N., Temperton, B., Bolduc, B., Alberti, A., … Cruaud, C. (2019). Marine DNA Viral Macro- and Microdiversity from Pole to Pole. Cell, 177(5), 1109–1123.e14. doi:10.1016/j.cell.2019.03.040

Acknowledgements
Tara Oceans (that includes both the Tara Oceans and Tara Oceans Polar Circle expeditions) would not exist without the leadership of the Tara Expeditions Foundation and the continuous support of 23 institutes (https://oceans.taraexpeditions.org). We further thank the commitment of the following sponsors: CNRS (in particular Groupement de Recherche GDR3280 and the Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans-GOSEE), European Molecular Biology Laboratory (EMBL), Genoscope/CEA, The French Ministry of Research, and 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), and PSL∗ Research University (ANR-11-IDEX-0001-02). We also thank the support and commitment of Agnès b. and Etienne Bourgois, the Prince Albert II de Monaco Foundation, the Veolia Foundation, Region Bretagne, Lorient Agglomeration, Serge Ferrari, Worldcourier, and KAUST. The global sampling effort was enabled by countless scientists and crew who sampled aboard the Tara from 2009–2013, and we thank MERCATOR-CORIOLIS and ACRI-ST for providing daily satellite data during the expeditions. We are also grateful to the countries who graciously granted sampling permissions. The authors declare that all data reported herein are fully and freely available from the date of publication, with no restrictions, and that all of the analyses, publications, and ownership of data are free from legal entanglement or restriction by the various nations whose waters the Tara Oceans expeditions sampled in. This article is contribution number 86 of Tara Oceans. Computational support was provided by an award from the Ohio Supercomputer Center (OSC) to M.B.S. Study design and manuscript comments from Bonnie T. Poulos, Ho Bin Jang, M. Consuelo Gazitúa, Olivier Zablocki, Janaina Rigonato, Damien Eveillard, Frédéric Mahé, Federico Ibarbalz, and Hisashi Endo are gratefully acknowledged. Funding was provided by the Gordon and Betty Moore Foundation (3790 to M.B.S.), NSF (OCE 1536989 and OCE 1829831 to M.B.S.), Oceanomics (ANR-11-BTBR-0008) and France Genomique (ANR-10-INBS-09) to Genoscope, ETH and Helmut Horten Foundation (to S.S.), a Netherlands Organization for Scientific Research (NWO) Vidi grant (864.14.004 to B.E.D.), and an NIH T32 training grant fellowship (AI112542 to A.C.G.). M.B. C.B. and L.K.-B. directed the Tara Oceans Polar Circle expedition. M.C. C.D. J.F. S.K. C.M. S. Pesant, M.P. S. Pisarev, J.P. and Tara Oceans coordinators conceptualized and organized sampling efforts for the Tara Oceans Polar Circle expedition. S. Pesant annotated, curated, and managed all biogeochemical data. A.A. C.C. and P.W. coordinated all sequencing efforts. A.C.G. A.A.Z. N.C.-N. B.T. B.B. K.A. G.D.-H.Y.L. D.V. J.-E.T. M.B. C.B. C.d.V. A.I.C. B.E.D. D.I. L.K.-B. S.R. S.S. P.W. and M.B.S. created the study design, analyzed the data, and wrote the manuscript. All authors approved the final manuscript. The authors declare no competing interests.

Publisher
Elsevier BV

Journal
Cell

DOI
10.1016/j.cell.2019.03.040

Additional Links
https://linkinghub.elsevier.com/retrieve/pii/S0092867419303411

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