Cryptic and abundant marine viruses at the evolutionary origins of Earth’s RNA virome

Author:

Zayed Ahmed A.123ORCID,Wainaina James M.13ORCID,Dominguez-Huerta Guillermo123ORCID,Pelletier Eric45ORCID,Guo Jiarong123ORCID,Mohssen Mohamed136ORCID,Tian Funing13ORCID,Pratama Akbar Adjie12ORCID,Bolduc Benjamin123ORCID,Zablocki Olivier123,Cronin Dylan123ORCID,Solden Lindsey1,Delage Erwan57ORCID,Alberti Adriana45ORCID,Aury Jean-Marc45ORCID,Carradec Quentin45ORCID,da Silva Corinne45ORCID,Labadie Karine45ORCID,Poulain Julie45ORCID,Ruscheweyh Hans-Joachim8ORCID,Salazar Guillem8,Shatoff Elan9ORCID,Bundschuh Ralf691011ORCID,Fredrick Kurt1ORCID,Kubatko Laura S.1213,Chaffron Samuel57ORCID,Culley Alexander I.14ORCID,Sunagawa Shinichi8ORCID,Kuhn Jens H.15ORCID,Wincker Patrick45,Sullivan Matthew B.123612ORCID,Acinas Silvia G.,Babin Marcel,Bork Peer,Boss Emmanuel,Bowler Chris,Cochrane Guy,de Vargas Colomban,Gorsky Gabriel,Guidi Lionel,Grimsley Nigel,Hingamp Pascal,Iudicone Daniele,Jaillon Olivier,Kandels Stefanie,Karp-Boss Lee,Karsenti Eric,Not Fabrice,Ogata Hiroyuki,Poulton Nicole,Pesant Stéphane,Sardet Christian,Speich Sabrinia,Stemmann Lars,Sullivan Matthew B.,Sungawa Shinichi,Wincker Patrick,

Affiliation:

1. Department of Microbiology, Ohio State University, Columbus, OH 43210, USA.

2. EMERGE Biology Integration Institute, Ohio State University, Columbus, OH 43210, USA.

3. Center of Microbiome Science, Ohio State University, Columbus, OH 43210, USA.

4. Génomique Métabolique, Genoscope, Institut François-Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91000 Evry, France.

5. Research Federation for the Study of Global Ocean Systems Ecology and Evolution, FR2022/Tara Oceans GOSEE, 75016 Paris, France.

6. The Interdisciplinary Biophysics Graduate Program, Ohio State University, Columbus, OH 43210, USA.

7. Nantes Université, CNRS UMR 6004, LS2N, F-44000 Nantes, France.

8. Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zurich, Zurich, Switzerland.

9. Department of Physics, Ohio State University, Columbus, OH 43210, USA.

10. Department of Chemistry and Biochemistry, Ohio State University, Columbus, OH 43210, USA.

11. Division of Hematology, Department of Internal Medicine, Ohio State University, Columbus, OH 43210, USA.

12. Department of Evolution, Ecology, and Organismal Biology, Ohio State University, Columbus, OH 43210, USA.

13. Department of Statistics, Ohio State University, Columbus, OH 43210, USA.

14. Département de Biochimie, Microbiologie et Bio-informatique, Université Laval, Québec, Québec G1V 0A6, Canada.

15. Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Fort Detrick, Frederick, MD 21702, USA.

Abstract

Whereas DNA viruses are known to be abundant, diverse, and commonly key ecosystem players, RNA viruses are insufficiently studied outside disease settings. In this study, we analyzed ≈28 terabases of Global Ocean RNA sequences to expand Earth’s RNA virus catalogs and their taxonomy, investigate their evolutionary origins, and assess their marine biogeography from pole to pole. Using new approaches to optimize discovery and classification, we identified RNA viruses that necessitate substantive revisions of taxonomy (doubling phyla and adding >50% new classes) and evolutionary understanding. “Species”-rank abundance determination revealed that viruses of the new phyla “ Taraviricota ,” a missing link in early RNA virus evolution, and “ Arctiviricota ” are widespread and dominant in the oceans. These efforts provide foundational knowledge critical to integrating RNA viruses into ecological and epidemiological models.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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