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Cell. 2019 May 16;177(5):1109-1123.e14. doi: 10.1016/j.cell.2019.03.040. Epub 2019 Apr 25.

Marine DNA Viral Macro- and Microdiversity from Pole to Pole.

Author information

1
Department of Microbiology, The Ohio State University, Columbus, OH 43210, USA.
2
Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory of Viral Metagenomics, KU Leuven-University of Leuven, Leuven, Belgium; Department of Microbiology and Immunology, Rega Institute for Medical Research, Laboratory for Clinical and Epidemiological Virology, KU Leuven-University of Leuven, Leuven, Belgium.
3
School of Biosciences, University of Exeter, Exeter, UK.
4
Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France; Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France.
5
Sorbonne Université, CNRS, Laboratoire d'Océanographie de Villefanche, LOV, 06230 Villefranche-sur-mer, France.
6
Theoretical Biology and Bioinformatics, Utrecht University, Utrecht, the Netherlands.
7
Sorbonne Université, CNRS, Station Biologique de Roscoff, AD2M ECOMAP, 29680 Roscoff, France; Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France.
8
CEA-Institut de Biologie François Jacob, Genoscope, Evry 91057, France; Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France.
9
Sorbonne Université, CNRS, Laboratoire d'Océanographie de Villefanche, LOV, 06230 Villefranche-sur-mer, France; Institut de Biologie de l'ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France; Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France.
10
Département de biologie, Québec Océan and Takuvik Joint International Laboratory (UMI 3376), Université Laval (Canada)-CNRS (France), Université Laval, Québec, QC G1V 0A6, Canada.
11
Structural and Computational Biology, European Molecular Biology Laboratory, 69117 Heidelberg, Germany; Directors' Research, European Molecular Biology Laboratory, 69117 Heidelberg, Germany.
12
PANGAEA, Data Publisher for Earth and Environmental Science, University of Bremen, 28359 Bremen, Germany; MARUM, Bremen University, 28359 Bremen, Germany.
13
Sorbonne Université, CNRS, Laboratoire d'Océanographie de Villefanche, LOV, 06230 Villefranche-sur-mer, France; Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France.
14
Shirshov Institute of Oceanology of Russian Academy of Sciences, 36 Nakhimovsky prosp, 117997 Moscow, Russia.
15
Institut de Biologie de l'ENS (IBENS), Département de biologie, École normale supérieure, CNRS, INSERM, Université PSL, 75005 Paris, France; Research Federation for the study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 3 rue Michel-Ange, 75016 Paris, France.
16
Département de biochimie, microbiologie et bio-informatique, Université Laval, Québec, QC G1V 0A6, Canada.
17
Theoretical Biology and Bioinformatics, Utrecht University, Utrecht, the Netherlands; Centre for Molecular and Biomolecular Informatics, Radboud University Medical Centre, Nijmegen, the Netherlands.
18
Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy.
19
School of Marine Sciences, University of Maine, Orono, ME, USA.
20
Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zurich, 8093 Zurich, Switzerland.
21
Department of Microbiology, The Ohio State University, Columbus, OH 43210, USA; Department of Civil, Environmental and Geodetic Engineering, The Ohio State University, Columbus, OH 43210, USA. Electronic address: mbsulli@gmail.com.

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.

KEYWORDS:

community ecology; diversity gradients; marine biology; metagenomics; population ecology; species; viruses

PMID:
31031001
PMCID:
PMC6525058
[Available on 2020-05-16]
DOI:
10.1016/j.cell.2019.03.040

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