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

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

Research output: Contribution to journal › Article › Research › peer-review

121 Citations (Scopus)

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.

Original language	English
Pages (from-to)	4023-4037.e18
Number of pages	34
Journal	Cell
Volume	185
Issue number	21
DOIs	https://doi.org/10.1016/j.cell.2022.08.023
Publication status	Published - 13 Oct 2022
Externally published	Yes

Keywords

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

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10.1016/j.cell.2022.08.023Licence: CC BY-NC-ND

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Neri, U., Wolf, Y. I., Roux, S., Camargo, A. P., Lee, B., Kazlauskas, D., Chen, I. M., Ivanova, N., Zeigler Allen, L., Paez-Espino, D., Bryant, D. A., Bhaya, D., RNA Virus Discovery Consortium, Krupovic, M., Dolja, V. V., Kyrpides, N. C., Koonin, E. V., & Gophna, U. (2022). Expansion of the global RNA virome reveals diverse clades of bacteriophages. Cell, 185(21), 4023-4037.e18. https://doi.org/10.1016/j.cell.2022.08.023

@article{d6e39d61025c41829eae15eb10e38d63,

title = "Expansion of the global RNA virome reveals diverse clades of bacteriophages",

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 dependent RNA polymerase, RNA Virus, Viral Ecology, viral phylogeny, Virus, Virus - Host prediction",

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

note = "Funding Information: The authors would like to thank Shai Zilberzwige-Tal, David Burstein, Adi Stern, Leah Reshef, and Omry Lieber for helpful discussions. U.G. and U.N. are supported by the European Research Council ( ERC-AdG 787514 ). U.N. is supported by a fellowship from the Edmond J. Safra Center for Bioinformatics at Tel Aviv University. Y.I.W. and E.V.K. are supported through the Intramural Research Program of the US National Institutes of Health (National Library of Medicine). V.V.D. was partially supported by NIH/NLM/NCBI Visiting Scientist Fellowship. The work of the U.S. Department of Energy Joint Genome Institute (S.R., A.P.C., I.M.C., N.I., D.P.-E., N.C.K., and all JGI co-authors), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy under contract no. DE-AC02-05CH11231 . M.K. was supported by l{\textquoteright}Agence Nationale de la Recherche grants ANR-20-CE20-009-02 and ANR-21-CE11-0001-01. D.K. was funded by the European Social Fund under no. 09.3.3- LMT-K-712-14-0027 . D.A.B. is supported by grant NNX16SJ62G from the NASA Exobiology program , and by grant DE-FG02-94ER20137 from the Photosynthetic Systems Program , Division of Chemical Sciences, Geosciences, and Biosciences (CSGB), Office of Basic Energy Sciences of the U.S. Department of Energy . We gratefully acknowledge the contributions of many scientists and principal investigators, who sent extracted genetic material for isolate genomes, environmental metagenomes, and metatranscriptomes, or sequencing results as part of the Department of Energy Joint Genome Institute Community Science Program and allowed us to include in our study the RNA virus sequences detected in these publicly available data sets regardless of publication status. Publisher Copyright: {\textcopyright} 2022 The Authors",

year = "2022",

month = oct,

day = "13",

doi = "10.1016/j.cell.2022.08.023",

language = "English",

volume = "185",

pages = "4023--4037.e18",

journal = "Cell",

issn = "0092-8674",

publisher = "Cell Press",

number = "21",

}

Neri, U, Wolf, YI, Roux, S, Camargo, AP, Lee, B, Kazlauskas, D, Chen, IM, Ivanova, N, Zeigler Allen, L, Paez-Espino, D, Bryant, DA, Bhaya, D, RNA Virus Discovery Consortium, Krupovic, M, Dolja, VV, Kyrpides, NC, Koonin, EV & Gophna, U 2022, 'Expansion of the global RNA virome reveals diverse clades of bacteriophages', Cell, vol. 185, no. 21, pp. 4023-4037.e18. https://doi.org/10.1016/j.cell.2022.08.023

TY - JOUR

T1 - Expansion of the global RNA virome reveals diverse clades of bacteriophages

AU - Neri, Uri

AU - Wolf, Yuri I.

AU - Roux, Simon

AU - Camargo, Antonio Pedro

AU - Lee, Benjamin

AU - Kazlauskas, Darius

AU - Chen, I. Min

AU - Ivanova, Natalia

AU - Zeigler Allen, Lisa

AU - Paez-Espino, David

AU - Bryant, Donald A.

AU - Bhaya, Devaki

AU - Narrowe, Adrienne B.

AU - Probst, Alexander J.

AU - Sczyrba, Alexander

AU - Kohler, Annegret

AU - Séguin, Armand

AU - Shade, Ashley

AU - Campbell, Barbara J.

AU - Lindahl, Björn D.

AU - Reese, Brandi Kiel

AU - Roque, Breanna M.

AU - DeRito, Chris

AU - Averill, Colin

AU - Cullen, Daniel

AU - Beck, David A.C.

AU - Walsh, David A.

AU - Ward, David M.

AU - Wu, Dongying

AU - Eloe-Fadrosh, Emiley

AU - Brodie, Eoin L.

AU - Young, Erica B.

AU - Lilleskov, Erik A.

AU - Castillo, Federico J.

AU - Martin, Francis M.

AU - LeCleir, Gary R.

AU - Attwood, Graeme T.

AU - Cadillo-Quiroz, Hinsby

AU - Simon, Holly M.

AU - Hewson, Ian

AU - Grigoriev, Igor V.

AU - Tiedje, James M.

AU - Jansson, Janet K.

AU - Lee, Janey

AU - VanderGheynst, Jean S.

AU - Dangl, Jeff

AU - Bowman, Jeff S.

AU - Blanchard, Jeffrey L.

AU - Bowen, Jennifer L.

AU - Xu, Jiangbing

AU - Banfield, Jillian F.

AU - Deming, Jody W.

AU - Kostka, Joel E.

AU - Gladden, John M.

AU - Rapp, Josephine Z.

AU - Sharpe, Joshua

AU - McMahon, Katherine D.

AU - Treseder, Kathleen K.

AU - Bidle, Kay D.

AU - Wrighton, Kelly C.

AU - Thamatrakoln, Kimberlee

AU - Nusslein, Klaus

AU - Meredith, Laura K.

AU - Ramirez, Lucia

AU - Buee, Marc

AU - Huntemann, Marcel

AU - Kalyuzhnaya, Marina G.

AU - Waldrop, Mark P.

AU - Sullivan, Matthew B.

AU - Schrenk, Matthew O.

AU - Hess, Matthias

AU - Vega, Michael A.

AU - O'Malley, Michelle A.

AU - Medina, Monica

AU - Gilbert, Naomi E.

AU - Delherbe, Nathalie

AU - Mason, Olivia U.

AU - Dijkstra, Paul

AU - Chuckran, Peter F.

AU - Baldrian, Petr

AU - Constant, Philippe

AU - Stepanauskas, Ramunas

AU - Daly, Rebecca A.

AU - Lamendella, Regina

AU - Gruninger, Robert J.

AU - McKay, Robert M.

AU - Hylander, Samuel

AU - Lebeis, Sarah L.

AU - Esser, Sarah P.

AU - Acinas, Silvia G.

AU - Wilhelm, Steven S.

AU - Singer, Steven W.

AU - Tringe, Susannah S.

AU - Woyke, Tanja

AU - Reddy, T. B.K.

AU - Bell, Terrence H.

AU - Mock, Thomas

AU - McAllister, Tim

AU - Thiel, Vera

AU - Denef, Vincent J.

AU - Liu, Wen Tso

AU - Martens-Habbena, Willm

AU - Allen Liu, Xiao Jun

AU - Cooper, Zachary S.

AU - Wang, Zhong

AU - RNA Virus Discovery Consortium

AU - Krupovic, Mart

AU - Dolja, Valerian V.

AU - Kyrpides, Nikos C.

AU - Koonin, Eugene V.

AU - Gophna, Uri

N1 - Funding Information: The authors would like to thank Shai Zilberzwige-Tal, David Burstein, Adi Stern, Leah Reshef, and Omry Lieber for helpful discussions. U.G. and U.N. are supported by the European Research Council ( ERC-AdG 787514 ). U.N. is supported by a fellowship from the Edmond J. Safra Center for Bioinformatics at Tel Aviv University. Y.I.W. and E.V.K. are supported through the Intramural Research Program of the US National Institutes of Health (National Library of Medicine). V.V.D. was partially supported by NIH/NLM/NCBI Visiting Scientist Fellowship. The work of the U.S. Department of Energy Joint Genome Institute (S.R., A.P.C., I.M.C., N.I., D.P.-E., N.C.K., and all JGI co-authors), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy under contract no. DE-AC02-05CH11231 . M.K. was supported by l’Agence Nationale de la Recherche grants ANR-20-CE20-009-02 and ANR-21-CE11-0001-01. D.K. was funded by the European Social Fund under no. 09.3.3- LMT-K-712-14-0027 . D.A.B. is supported by grant NNX16SJ62G from the NASA Exobiology program , and by grant DE-FG02-94ER20137 from the Photosynthetic Systems Program , Division of Chemical Sciences, Geosciences, and Biosciences (CSGB), Office of Basic Energy Sciences of the U.S. Department of Energy . We gratefully acknowledge the contributions of many scientists and principal investigators, who sent extracted genetic material for isolate genomes, environmental metagenomes, and metatranscriptomes, or sequencing results as part of the Department of Energy Joint Genome Institute Community Science Program and allowed us to include in our study the RNA virus sequences detected in these publicly available data sets regardless of publication status. Publisher Copyright: © 2022 The Authors

PY - 2022/10/13

Y1 - 2022/10/13

N2 - 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.

AB - 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.

KW - Bactriophage

KW - Functional protein annotation

KW - Metatranscriptomics

KW - RNA dependent RNA polymerase

KW - RNA Virus

KW - Viral Ecology

KW - viral phylogeny

KW - Virus

KW - Virus - Host prediction

UR - http://www.scopus.com/inward/record.url?scp=85138907493&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2022.08.023

DO - 10.1016/j.cell.2022.08.023

M3 - Article

C2 - 36174579

AN - SCOPUS:85138907493

SN - 0092-8674

VL - 185

SP - 4023-4037.e18

JO - Cell

JF - Cell

IS - 21

ER -

Expansion of the global RNA virome reveals diverse clades of bacteriophages

Abstract

Keywords

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