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Ecogenomics and biogeochemical impacts of uncultivated globally abundant ocean viruses

Simon Roux, Jennifer R. Brum, View ORCID ProfileBas E. Dutilh, View ORCID ProfileShinichi Sunagawa, View ORCID ProfileMelissa B. Duhaime, View ORCID ProfileAlexander Loy, Bonnie T. Poulos, Natalie Solonenko, View ORCID ProfileElena Lara, Julie Poulain, View ORCID ProfileStéphane Pesant, View ORCID ProfileStefanie Kandels-Lewis, Céline Dimier, Marc Picheral, Sarah Searson, Corinne Cruaud, Adriana Alberti, View ORCID ProfileCarlos M. Duarte, View ORCID ProfileJosep M. Gasol, View ORCID ProfileDolors Vaqué, Tara Oceans Coordinators, View ORCID ProfilePeer Bork, View ORCID ProfileSilvia G. Acinas, Patrick Wincker, Matthew B. Sullivan, Silvia G. Acinas, Peer Bork, Emmanuel Boss, Chris Bowler, Colomban de Vargas, Michael Follows, Gabriel Gorsky, Nigel Grimsley, Pascal Hingamp, Daniele Iudicone, Olivier Jaillon, Stefanie Kandels-Lewis, Lee Karp-Boss, Eric Karsenti, Uros Krzic, Fabrice Not, Hiroyuki Ogata, Stephane Pesant, Jeroen Raes, Emmanuel G. Reynaud, Christian Sardet, Mike Sieracki, Sabrina Speich, Lars Stemmann, Matthew B. Sullivan, Shinichi Sunagawa, Didier Velayoudon, Patrick Wincker
doi: https://doi.org/10.1101/053090
Simon Roux
1Department of Microbiology, The Ohio State University, Columbus, OH, USA
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Jennifer R. Brum
1Department of Microbiology, The Ohio State University, Columbus, OH, USA
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Bas E. Dutilh
2Theoretical Biology and Bioinformatics, Utrecht University, Utrecht, The Netherlands
3Centre for Molecular and Biomolecular Informatics, Radboud University Medical Centre, Nijmegen, The Netherlands
4Department of Marine Biology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
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  • ORCID record for Bas E. Dutilh
Shinichi Sunagawa
5Structural and Computational Biology, European Molecular Biology Laboratory, Heidelberg, Germany
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  • ORCID record for Shinichi Sunagawa
Melissa B. Duhaime
6Department of Ecology and Evolutionary Biology, University of Michigan, MI, USA
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  • ORCID record for Melissa B. Duhaime
Alexander Loy
7Division of Microbial Ecology, Department of Microbiology and Ecosystem Science, Research Network Chemistry Meets Microbiology, University of Vienna, Vienna, Austria
8Austrian Polar Research Institute, Vienna, Austria
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  • ORCID record for Alexander Loy
Bonnie T. Poulos
9Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, USA
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Natalie Solonenko
1Department of Microbiology, The Ohio State University, Columbus, OH, USA
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Elena Lara
10Department of Marine Biology and Oceanography, Institut de Ciències del Mar (CSIC), Barcelona, Spain
11Institute of Marine Sciences (CNR-ISMAR), National Research Council, Venezia, Italy
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  • ORCID record for Elena Lara
Julie Poulain
12CEA - Institut de Génomique, GENOSCOPE, Evry, France
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Stéphane Pesant
13PANGAEA, Data Publisher for Earth and Environmental Science, University of Bremen, Bremen, Germany
14MARUM, Bremen University, Bremen, Germany
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  • ORCID record for Stéphane Pesant
Stefanie Kandels-Lewis
5Structural and Computational Biology, European Molecular Biology Laboratory, Heidelberg, Germany
15Directors’ Research European Molecular Biology Laboratory, Heidelberg, Germany
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  • ORCID record for Stefanie Kandels-Lewis
Céline Dimier
16Sorbonne Universités, UPMC Université Paris 06, CNRS, Laboratoire Adaptation et Diversité en Milieu Marin, Station Biologique de Roscoff, Roscoff, France
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Marc Picheral
17Sorbonne Universités, UPMC Université Paris 06, CNRS, Laboratoire d’oceanographie de Villefranche (LOV), Observatoire Océanologique, Villefranche-sur-Mer, France
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Sarah Searson
17Sorbonne Universités, UPMC Université Paris 06, CNRS, Laboratoire d’oceanographie de Villefranche (LOV), Observatoire Océanologique, Villefranche-sur-Mer, France
18Department of Oceanography, University of Hawaii, Honolulu, Hawaii, USA
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Corinne Cruaud
12CEA - Institut de Génomique, GENOSCOPE, Evry, France
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Adriana Alberti
12CEA - Institut de Génomique, GENOSCOPE, Evry, France
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Carlos M. Duarte
19Mediterranean Institute of Advanced Studies, CSIC-UiB, Esporles, Mallorca, Spain
20King Abdullah University of Science and Technology (KAUST), Red Sea Research Center (RSRC), Thuwal, Saudi Arabia
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  • ORCID record for Carlos M. Duarte
Josep M. Gasol
10Department of Marine Biology and Oceanography, Institut de Ciències del Mar (CSIC), Barcelona, Spain
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  • ORCID record for Josep M. Gasol
Dolors Vaqué
10Department of Marine Biology and Oceanography, Institut de Ciències del Mar (CSIC), Barcelona, Spain
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  • ORCID record for Dolors Vaqué
Peer Bork
5Structural and Computational Biology, European Molecular Biology Laboratory, Heidelberg, Germany
21Max-Delbrück-Centre for Molecular Medicine, 13092 Berlin, Germany
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Silvia G. Acinas
10Department of Marine Biology and Oceanography, Institut de Ciències del Mar (CSIC), Barcelona, Spain
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  • ORCID record for Silvia G. Acinas
Patrick Wincker
12CEA - Institut de Génomique, GENOSCOPE, Evry, France
22CNRS, UMR 8030, CP5706, Evry, France
23Université d’Evry, UMR 8030, CP5706, Evry, France
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Matthew B. Sullivan
1Department of Microbiology, The Ohio State University, Columbus, OH, USA
24Department of Civil, Environmental and Geodetic Engineering, The Ohio State University, Columbus, OH, USA
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  • For correspondence: mbsulli@gmail.com
Silvia G. Acinas
1Department of Marine Biology and Oceanography Institute of Marine Science (ICM)-CSIC Pg. Marítim de la Barceloneta 37-49, Barcelona, E08003, Spain
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Peer Bork
2Structural and Computational Biology, European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany
3Max-Delbrück-Centre for Molecular Medicine, 13092 Berlin, Germany
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Emmanuel Boss
4School of Marine Sciences, University of Maine, Orono, Maine, USA
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Chris Bowler
5Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l’Ecole Normale Supérieure (IBENS), CNRS UMR 8197, INSERM U1024, 46 rue d’Ulm, F-75005 Paris, France
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Colomban de Vargas
6CNRS, UMR 7144, Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France
7Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France
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Michael Follows
8Dept of Earth, Atmospheric and Planetary Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA
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Gabriel Gorsky
9CNRS, UMR 7093, LOV, Observatoire Océanologique, F-06230 Villefranche-sur-mer, France
31Sorbonne Universités, UPMC Univ Paris 06, UMR 7093, LOV, Observatoire Océanologique, F-06230, Villefranche-sur-mer, France
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Nigel Grimsley
10CNRS UMR 7232, BIOM, Avenue du Fontaulé, 66650 Banyuls-sur-Mer, France
11Sorbonne Universités Paris 06, OOB UPMC, Avenue du Fontaulé, 66650 Banyuls-sur-Mer, France
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Pascal Hingamp
12Aix Marseille Université CNRS IGS UMR 7256 13288 Marseille, France
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Daniele Iudicone
13Stazione Zoologica Anton Dohrn, Villa Comunale, 80121, Naples, Italy
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Olivier Jaillon
14CEA - Institut de Génomique, GENOSCOPE, 2 rue Gaston Crémieux, 91057 Evry, France
15CNRS, UMR 8030, CP5706, Evry, France
16Université d’Evry, UMR 8030, CP5706, Evry, France
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Stefanie Kandels-Lewis
2Structural and Computational Biology, European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany
17Directors’ Research European Molecular Biology Laboratory Meyerhofstr. 1 69117 Heidelberg, Germany
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Lee Karp-Boss
18School of Marine Sciences, University of Maine, Orono, USA
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Eric Karsenti
5Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l’Ecole Normale Supérieure (IBENS), CNRS UMR 8197, INSERM U1024, 46 rue d’Ulm, F-75005 Paris, France
17Directors’ Research European Molecular Biology Laboratory Meyerhofstr. 1 69117 Heidelberg, Germany
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Uros Krzic
19Cell Biology and Biophysics, European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany
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Fabrice Not
6CNRS, UMR 7144, Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France
7Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France
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Hiroyuki Ogata
20Institute for Chemical Research, Kyoto University, Gokasho, Uji, Kyoto, 611-0011, Japan
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Stephane Pesant
21PANGAEA, Data Publisher for Earth and Environmental Science, University of Bremen, Bremen, Germany
22MARUM, Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany
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Jeroen Raes
23Department of Microbiology and Immunology, Rega Institute, KU Leuven, Herestraat 49, 3000 Leuven, Belgium
24Center for the Biology of Disease, VIB, Herestraat 49, 3000 Leuven, Belgium
25Department of Applied Biological Sciences, Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium
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Emmanuel G. Reynaud
26Earth Institute, University College Dublin, Dublin, Ireland
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Christian Sardet
27CNRS, UMR 7009 Biodev, Observatoire Océanologique, F-06230 Villefranche-sur-mer, France
28Sorbonne Universités, UPMC Univ Paris 06, UMR 7009 Biodev, F-06230 Observatoire Océanologique, Villefranche-sur-mer, France
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Mike Sieracki
29Bigelow Laboratory for Ocean Science, East Boothbay, Maine, USA
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Sabrina Speich
30Laboratoire de Physique des Océan UBO-IUEM Palce Copernic 29820 Polouzané, France
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Lars Stemmann
9CNRS, UMR 7093, LOV, Observatoire Océanologique, F-06230 Villefranche-sur-mer, France
31Sorbonne Universités, UPMC Univ Paris 06, UMR 7093, LOV, Observatoire Océanologique, F-06230, Villefranche-sur-mer, France
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Matthew B. Sullivan
32Department of Ecology and Evolutionary Biology, Depts Molecular and Cellular Biology and Soil, Water and Environmental Science, University of Arizona, Tucson, Arizona, 85721, USA
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Shinichi Sunagawa
2Structural and Computational Biology, European Molecular Biology Laboratory, Meyerhofstr. 1, 69117 Heidelberg, Germany
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Didier Velayoudon
33DVIP Consulting, 92310, Sèvres, France
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Patrick Wincker
14CEA - Institut de Génomique, GENOSCOPE, 2 rue Gaston Crémieux, 91057 Evry, France
15CNRS, UMR 8030, CP5706, Evry, France
16Université d’Evry, UMR 8030, CP5706, Evry, France
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Abstract

Ocean microbes drive global-scale biogeochemical cycling1, but do so under constraints imposed by viruses on host community composition, metabolism, and evolutionary trajectories2–5. Due to sampling and cultivation challenges, genome-level viral diversity remains poorly described and grossly understudied in nature such that <1% of observed surface ocean viruses, even those that are abundant and ubiquitous, are ‘known’5. Here we analyze a global map of abundant, double stranded DNA (dsDNA) viruses and viral-encoded auxiliary metabolic genes (AMGs) with genomic and ecological contexts through the Global Ocean Viromes (GOV) dataset, which includes complete genomes and large genomic fragments from both surface and deep ocean viruses sampled during the Tara Oceans and Malaspina research expeditions6,7. A total of 15,222 epi- and mesopelagic viral populations were identified that comprised 867 viral clusters (VCs, approximately genus-level groups8,9). This roughly triples known ocean viral populations10, doubles known candidate bacterial and archaeal virus genera9, and near-completely samples epipelagic communities at both the population and VC level. Thirty-eight of the 867 VCs were identified as the most impactful dsDNA viral groups in the oceans, as these were locally or globally abundant and accounted together for nearly half of the viral populations in any GOV sample. Most of these were predicted in silico to infect dominant, ecologically relevant microbes, while two thirds of them represent newly described viruses that lacked any cultivated representative. Beyond these taxon-specific ecological observations, we identified 243 viral-encoded AMGs in GOV, only 95 of which were known. Deeper analyses of 4 of these AMGs revealed that abundant viruses directly manipulate sulfur and nitrogen cycling, and do so throughout the epipelagic ocean. Together these data provide a critically-needed organismal catalog and functional context to begin meaningfully integrating viruses into ecosystem models as key players in nutrient cycling and trophic networks.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Ecogenomics and biogeochemical impacts of uncultivated 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, Stéphane Pesant, Stefanie Kandels-Lewis, Céline Dimier, Marc Picheral, Sarah Searson, Corinne Cruaud, Adriana Alberti, Carlos M. Duarte, Josep M. Gasol, Dolors Vaqué, Tara Oceans Coordinators, Peer Bork, Silvia G. Acinas, Patrick Wincker, Matthew B. Sullivan, Silvia G. Acinas, Peer Bork, Emmanuel Boss, Chris Bowler, Colomban de Vargas, Michael Follows, Gabriel Gorsky, Nigel Grimsley, Pascal Hingamp, Daniele Iudicone, Olivier Jaillon, Stefanie Kandels-Lewis, Lee Karp-Boss, Eric Karsenti, Uros Krzic, Fabrice Not, Hiroyuki Ogata, Stephane Pesant, Jeroen Raes, Emmanuel G. Reynaud, Christian Sardet, Mike Sieracki, Sabrina Speich, Lars Stemmann, Matthew B. Sullivan, Shinichi Sunagawa, Didier Velayoudon, Patrick Wincker
bioRxiv 053090; doi: https://doi.org/10.1101/053090
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Ecogenomics and biogeochemical impacts of uncultivated 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, Stéphane Pesant, Stefanie Kandels-Lewis, Céline Dimier, Marc Picheral, Sarah Searson, Corinne Cruaud, Adriana Alberti, Carlos M. Duarte, Josep M. Gasol, Dolors Vaqué, Tara Oceans Coordinators, Peer Bork, Silvia G. Acinas, Patrick Wincker, Matthew B. Sullivan, Silvia G. Acinas, Peer Bork, Emmanuel Boss, Chris Bowler, Colomban de Vargas, Michael Follows, Gabriel Gorsky, Nigel Grimsley, Pascal Hingamp, Daniele Iudicone, Olivier Jaillon, Stefanie Kandels-Lewis, Lee Karp-Boss, Eric Karsenti, Uros Krzic, Fabrice Not, Hiroyuki Ogata, Stephane Pesant, Jeroen Raes, Emmanuel G. Reynaud, Christian Sardet, Mike Sieracki, Sabrina Speich, Lars Stemmann, Matthew B. Sullivan, Shinichi Sunagawa, Didier Velayoudon, Patrick Wincker
bioRxiv 053090; doi: https://doi.org/10.1101/053090

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