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; Mart Krupovic; Valerian V. Dolja; Nikos C. Kyrpides; Eugene V. Koonin; Uri Gophna; 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

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, Mart Krupovic, Valerian V. Dolja, Nikos C. Kyrpides, Eugene V. Koonin, Uri Gophna, Adrienne B. Narrowe, Alexander J. Probst, Alexander SczyrbaAnnegret 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

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

121 Citations (SciVal)

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	15
Journal	Cell
Volume	185
Issue number	21
Early online date	28 Sept 2022
DOIs	https://doi.org/10.1016/j.cell.2022.08.023
Publication status	Published - 13 Oct 2022

Keywords

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

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

1-s2.0-S0092867422011187-mainFinal published version, 6.23 MBLicence: 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., Krupovic, M., Dolja, V. V., Kyrpides, N. C., Koonin, E. V., Gophna, U., Narrowe, A. B., Probst, A. J., ... Wang, Z. (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

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

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 Mart Krupovic and Dolja, {Valerian V.} and Kyrpides, {Nikos C.} and Koonin, {Eugene V.} and Uri Gophna 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 Wen-Tso Liu and Willm Martens-Habbena and {Allen Liu}, Xiao-Jun and Cooper, {Zachary S.} and Zhong Wang",

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, Krupovic, M, Dolja, VV, Kyrpides, NC, Koonin, EV, Gophna, U, Narrowe, AB, Probst, AJ, Sczyrba, A, Kohler, A, Séguin, A, Shade, A, Campbell, BJ, Lindahl, BD, Reese, BK, Roque, BM, Derito, C, Averill, C, Cullen, D, Beck, DAC, Walsh, DA, Ward, DM, Wu, D, Eloe-Fadrosh, E, Brodie, EL, Young, EB, Lilleskov, EA, Castillo, FJ, Martin, FM, Lecleir, GR, Attwood, GT, Cadillo-Quiroz, H, Simon, HM, Hewson, I, Grigoriev, IV, Tiedje, JM, Jansson, JK, Lee, J, Vandergheynst, JS, Dangl, J, Bowman, JS, Blanchard, JL, Bowen, JL, Xu, J, Banfield, JF, Deming, JW, Kostka, JE, Gladden, JM, Rapp, JZ, Sharpe, J, McMahon, KD, Treseder, KK, Bidle, KD, Wrighton, KC, Thamatrakoln, K, Nusslein, K, Meredith, LK, Ramirez, L, Buee, M, Huntemann, M, Kalyuzhnaya, MG, Waldrop, MP, Sullivan, MB, Schrenk, MO, Hess, M, Vega, MA, O'Malley, MA, Medina, M, Gilbert, NE, Delherbe, N, Mason, OU, Dijkstra, P, Chuckran, PF, Baldrian, P, Constant, P, Stepanauskas, R, Daly, RA, Lamendella, R, Gruninger, RJ, Mckay, RM, Hylander, S, Lebeis, SL, Esser, SP, Acinas, SG, Wilhelm, SS, Singer, SW, Tringe, SS, Woyke, T, Reddy, TBK, Bell, TH, Mock, T, McAllister, T, Thiel, V, Denef, VJ, Liu, W-T, Martens-Habbena, W, Allen Liu, X-J, Cooper, ZS & Wang, Z 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 - Krupovic, Mart

AU - Dolja, Valerian V.

AU - Kyrpides, Nikos C.

AU - Koonin, Eugene V.

AU - Gophna, Uri

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

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 Virus

KW - RNA dependent RNA polymerase

KW - Viral Ecology

KW - Virus

KW - Virus - Host prediction

KW - viral phylogeny

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

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

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Keywords

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