Expansion of the global RNA virome reveals diverse clades of bacteriophages

Uri Neri; Yuri I Wolf; Simon Roux; Antonio Pedro Camargo; Benjamin Lee; Darius Kazlauskas; I Min Chen; Natalia Ivanova; Lisa Zeigler Allen; David Paez-Espino; Donald A Bryant; Devaki Bhaya; RNA Virus Discovery Consortium; Mart Krupovic; Valerian V Dolja; Nikos C Kyrpides; Eugene V Koonin; Uri Gophna

doi:10.1016/j.cell.2022.08.023

Expansion of the global RNA virome reveals diverse clades of bacteriophages

Cell. 2022 Oct 13;185(21):4023-4037.e18. doi: 10.1016/j.cell.2022.08.023. Epub 2022 Sep 28.

Authors

Uri Neri¹, Yuri I Wolf², Simon Roux³, Antonio Pedro Camargo³, Benjamin Lee⁴, Darius Kazlauskas⁵, I Min Chen³, Natalia Ivanova³, Lisa Zeigler Allen⁶, David Paez-Espino³, Donald A Bryant⁷, Devaki Bhaya⁸; RNA Virus Discovery Consortium; Mart Krupovic⁹, Valerian V Dolja¹⁰, Nikos C Kyrpides¹¹, Eugene V Koonin¹², Uri Gophna¹³

Collaborators

RNA Virus Discovery Consortium:
Adrienne B Narrowe, Alexander J Probst, Alexander Sczyrba, Annegret Kohler, Armand Séguin, Ashley Shade, Barbara J Campbell, Björn D Lindahl, Brandi Kiel Reese, Breanna M Roque, Chris DeRito, Colin Averill, Daniel Cullen, David A C Beck, David A Walsh, David M Ward, Dongying Wu, Emiley Eloe-Fadrosh, Eoin L Brodie, Erica B Young, Erik A Lilleskov, Federico J Castillo, Francis M Martin, Gary R LeCleir, Graeme T Attwood, Hinsby Cadillo-Quiroz, Holly M Simon, Ian Hewson, Igor V Grigoriev, James M Tiedje, Janet K Jansson, Janey Lee, Jean S VanderGheynst, Jeff Dangl, Jeff S Bowman, Jeffrey L Blanchard, Jennifer L Bowen, Jiangbing Xu, Jillian F Banfield, Jody W Deming, Joel E Kostka, John M Gladden, Josephine Z Rapp, Joshua Sharpe, Katherine D McMahon, Kathleen K Treseder, Kay D Bidle, Kelly C Wrighton, Kimberlee Thamatrakoln, Klaus Nusslein, Laura K Meredith, Lucia Ramirez, Marc Buee, Marcel Huntemann, Marina G Kalyuzhnaya, Mark P Waldrop, Matthew B Sullivan, Matthew O Schrenk, Matthias Hess, Michael A Vega, Michelle A O'Malley, Monica Medina, Naomi E Gilbert, Nathalie Delherbe, Olivia U Mason, Paul Dijkstra, Peter F Chuckran, Petr Baldrian, Philippe Constant, Ramunas Stepanauskas, Rebecca A Daly, Regina Lamendella, Robert J Gruninger, Robert M McKay, Samuel Hylander, Sarah L Lebeis, Sarah P Esser, Silvia G Acinas, Steven S Wilhelm, Steven W Singer, Susannah S Tringe, Tanja Woyke, T B K Reddy, Terrence H Bell, Thomas Mock, Tim McAllister, Vera Thiel, Vincent J Denef, Wen-Tso Liu, Willm Martens-Habbena, Xiao-Jun Allen Liu, Zachary S Cooper, Zhong Wang

Affiliations

¹ The Shmunis School of Biomedicine and Cancer Research, Tel Aviv University, Tel Aviv 6997801, Israel. Electronic address: uri.neri@gmail.com.
² National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA.
³ Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
⁴ National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA; Nuffield Department of Medicine, University of Oxford, Oxford OX3 7BN, UK.
⁵ Institute of Biotechnology, Life Sciences Center, Vilnius University, Saulėtekio av. 7, Vilnius 10257, Lithuania.
⁶ Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, USA; Marine Biology Research Division, Scripps Institution of Oceanography, La Jolla, CA, USA.
⁷ Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA 16802, USA.
⁸ Department of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305, USA.
⁹ Institut Pasteur, Université Paris Cité, CNRS UMR 6047, Archaeal Virology Unit, 75015 Paris, France.
¹⁰ National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA; Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA. Electronic address: doljav@oregonstate.edu.
¹¹ Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA. Electronic address: nckyrpides@lbl.gov.
¹² National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA. Electronic address: koonin@ncbi.nlm.nih.gov.
¹³ The Shmunis School of Biomedicine and Cancer Research, Tel Aviv University, Tel Aviv 6997801, Israel. Electronic address: urigo@tauex.tau.ac.il.

PMID: 36174579
DOI: 10.1016/j.cell.2022.08.023

Abstract

High-throughput RNA sequencing offers broad opportunities to explore the Earth RNA virome. Mining 5,150 diverse metatranscriptomes uncovered >2.5 million RNA virus contigs. Analysis of >330,000 RNA-dependent RNA polymerases (RdRPs) shows that this expansion corresponds to a 5-fold increase of the known RNA virus diversity. Gene content analysis revealed multiple protein domains previously not found in RNA viruses and implicated in virus-host interactions. Extended RdRP phylogeny supports the monophyly of the five established phyla and reveals two putative additional bacteriophage phyla and numerous putative additional classes and orders. The dramatically expanded phylum Lenarviricota, consisting of bacterial and related eukaryotic viruses, now accounts for a third of the RNA virome. Identification of CRISPR spacer matches and bacteriolytic proteins suggests that subsets of picobirnaviruses and partitiviruses, previously associated with eukaryotes, infect prokaryotic hosts.

Keywords: Bactriophage; Functional protein annotation; Metatranscriptomics; RNA Virus; RNA dependent RNA polymerase; Viral Ecology; Virus; Virus - Host prediction; viral phylogeny.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, N.I.H., Extramural
Research Support, N.I.H., Intramural

MeSH terms

Bacteriophages* / genetics
DNA-Directed RNA Polymerases / genetics
Genome, Viral
Phylogeny
RNA
RNA Viruses* / genetics
RNA-Dependent RNA Polymerase / genetics
Virome

Substances

RNA
RNA-Dependent RNA Polymerase
DNA-Directed RNA Polymerases