Abstract

Current knowledge of RNA virus biodiversity is both biased and fragmentary, reflecting a focus on culturable or disease-causing agents. Here we profile the transcriptomes of over 220 invertebrate species sampled across nine animal phyla and report the discovery of 1,445 RNA viruses, including some that are sufficiently divergent to comprise new families. The identified viruses fill major gaps in the RNA virus phylogeny and reveal an evolutionary history that is characterized by both host switching and co-divergence. The invertebrate virome also reveals remarkable genomic flexibility that includes frequent recombination, lateral gene transfer among viruses and hosts, gene gain and loss, and complex genomic rearrangements. Together, these data present a view of the RNA virosphere that is more phylogenetically and genomically diverse than that depicted in current classification schemes and provide a more solid foundation for studies in virus ecology and evolution.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Accessions

Primary accessions

BioProject

NCBI Reference Sequence

References

  1. 1.

    , & The ancient Virus World and evolution of cells. Biol. Direct 1, 29 (2006)

  2. 2.

    & Virus discovery and recent insights into virus diversity in arthropods. Curr. Opin. Microbiol. 16, 507–513 (2013)

  3. 3.

    et al. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife 4, e05378 (2015)

  4. 4.

    , , & Discovery and initial analysis of novel viral genomes in the soybean cyst nematode. J. Gen. Virol. 92, 1870–1879 (2011)

  5. 5.

    , , , & Discovery and evolution of bunyavirids in arctic phantom midges and ancient bunyavirid-like sequences in insect genomes. J. Virol. 88, 8783–8794 (2014)

  6. 6.

    et al. A tick-borne segmented RNA virus contains genome segments derived from unsegmented viral ancestors. Proc. Natl Acad. Sci. USA 111, 6744–6749 (2014)

  7. 7.

    et al. Virome analysis of Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis ticks reveals novel highly divergent vertebrate and invertebrate viruses. J. Virol. 88, 11480–11492 (2014)

  8. 8.

    et al. The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. PLoS Biol. 13, e1002210 (2015)

  9. 9.

    et al. Divergent viruses discovered in arthropods and vertebrates revise the evolutionary history of the Flaviviridae and related viruses. J. Virol. 90, 659–669 (2015)

  10. 10.

    The Evolution and Emergence of RNA Viruses. (Oxford Univ. Press, 2009)

  11. 11.

    The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 72, 2197–2206 (1991)

  12. 12.

    & Endogenous viruses: insights into viral evolution and impact on host biology. Nat. Rev. Genet. 13, 283–296 (2012)

  13. 13.

    , & Multigene analyses of bilaterian animals corroborate the monophyly of Ecdysozoa, Lophotrochozoa, and Protostomia. Mol. Biol. Evol. 22, 1246–1253 (2005)

  14. 14.

    , , & Virus Taxonomy: 9th Report of the International Committee on Taxonomy of Viruses. (Elsevier Academic Press, 2012)

  15. 15.

    et al. Viral load estimation in asymptomatic honey bee colonies using the quantitative RT–PCR technique. Apidologie (Celle) 38, 426–435 (2007)

  16. 16.

    et al. The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie (Celle) 41, 332–352 (2010)

  17. 17.

    et al. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Appl. Environ. Microbiol. 70, 7185–7191 (2004)

  18. 18.

    , & Evolution of cell recognition by viruses. Science 292, 1102–1105 (2001)

  19. 19.

    & Origins of mitochondria and hydrogenosomes. Curr. Opin. Microbiol. 2, 535–541 (1999)

  20. 20.

    , & Mitochondrial evolution. Science 283, 1476–1481 (1999)

  21. 21.

    A theory of modular evolution for bacteriophages. Ann. NY Acad. Sci. 354, 484–490 (1980)

  22. 22.

    Viruses in the sea. Nature 437, 356–361 (2005)

  23. 23.

    et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011)

  24. 24.

    & Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012)

  25. 25.

    , & Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 14, 178–192 (2013)

  26. 26.

    , , , & RNA-seq gene expression estimation with read mapping uncertainty. Bioinformatics 26, 493–500 (2010)

  27. 27.

    & MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013)

  28. 28.

    , & trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973 (2009)

  29. 29.

    , , & ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164–1165 (2011)

  30. 30.

    & A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696–704 (2003)

Download references

Acknowledgements

This study was supported by the National Natural Science Foundation of China (Grants 81290343, 81273014, 81672057), the Special National Project on Research and Development of Key Biosafety Technologies (Grants 2016YFC1201900, 2016YFC1200101), the 12th Five-Year Major National Science and Technology Projects of China (2014ZX10004001-005), and an NHMRC Australia Fellowship (GNT1037231).

Author information

Author notes

    • Mang Shi
    • , Xian-Dan Lin
    • , Jun-Hua Tian
    • , Liang-Jun Chen
    • , Xiao Chen
    •  & Ci-Xiu Li

    These authors contributed equally to this work.

Affiliations

  1. State Key Laboratory for Infectious Disease Prevention and Control, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Changping, 100206 Beijing, China

    • Mang Shi
    • , Liang-Jun Chen
    • , Ci-Xiu Li
    • , Xin-Cheng Qin
    • , Wen Wang
    • , Jianguo Xu
    • , Edward C. Holmes
    •  & Yong-Zhen Zhang
  2. Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, the University of Sydney, Sydney, New South Wales 2006, Australia

    • Mang Shi
    • , John-Sebastian Eden
    • , Jan Buchmann
    •  & Edward C. Holmes
  3. Wenzhou Center for Disease Control and Prevention, Wenzhou, 325001 Zhejiang, China

    • Xian-Dan Lin
  4. Wuhan Center for Disease Control and Prevention, Wuhan, 430015 Hubei, China

    • Jun-Hua Tian
  5. Guangxi Mangrove Research Center, Beihai, 536000 Guangxi, China

    • Xiao Chen
  6. Systems Biology and Bioinformatics Group, School of Biological Sciences, Faculty of Sciences, University of Hong Kong, Hong Kong, China

    • Jun Li
  7. National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, Shanghai, China

    • Jian-Ping Cao

Authors

  1. Search for Mang Shi in:

  2. Search for Xian-Dan Lin in:

  3. Search for Jun-Hua Tian in:

  4. Search for Liang-Jun Chen in:

  5. Search for Xiao Chen in:

  6. Search for Ci-Xiu Li in:

  7. Search for Xin-Cheng Qin in:

  8. Search for Jun Li in:

  9. Search for Jian-Ping Cao in:

  10. Search for John-Sebastian Eden in:

  11. Search for Jan Buchmann in:

  12. Search for Wen Wang in:

  13. Search for Jianguo Xu in:

  14. Search for Edward C. Holmes in:

  15. Search for Yong-Zhen Zhang in:

Contributions

Conceptualization: M.S. and Y.-Z.Z. Methodology: M.S., L.-J.C, C.-X.L., J.L., J.-S.E, J.B., E.C.H. and Y.-Z.Z. Investigation: M.S., X.-D.L., J.-H.T., L.-J.C, X.C., C.-X.L. and X.-C.Q. Writing (original draft): M.S., E.C.H. and Y.-Z.Z. Writing (review and editing): M.S., X.-D.L., J.-H.T., L.-J.C, X.C., C.-X.L, J.-S.E, J.X., E.C.H. and Y.-Z.Z. Funding Acquisition: J.X., E.C.H. and Y.-Z.Z. Resources (sampling): M.S., X.-D.L., J.-H.T., L.-J.C, X.C., C.-X.L., J.-P.C., W.W. and Y.-Z.Z. Resources (computational): M.S., J.L., J.B. and E.C.H. Supervision: E.C.H. and Y.-Z.Z.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Yong-Zhen Zhang.

Reviewer Information Nature thanks E. Ghedin, D. Obbard and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Data

    This file contains Supplementary Data 1-36, phylogenies and genome structures of each major virus clade. The phylogenies (SI data 1-21) contain detailed information on evolutionary relationships, the name of the viruses, the frequency of viral RNA, and the presence and location of endogenous virus elements (EVEs). The genome structures (SI data 22-36) contain information on the genome organization and the structural domains of representative viruses.

  2. 2.

    Supplementary Table 1

    This table contains the detailed information of each pool/library.

Excel files

  1. 1.

    Supplementary Table 2

    This table contains the detailed information on each virus discovered in this study.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature20167

Further reading

  • Numerous cultivated and uncultivated viruses encode ribosomal proteins

    • Carolina M. Mizuno
    • , Charlotte Guyomar
    • , Simon Roux
    • , Régis Lavigne
    • , Francisco Rodriguez-Valera
    • , Matthew B. Sullivan
    • , Reynald Gillet
    • , Patrick Forterre
    •  & Mart Krupovic

    Nature Communications (2019)

  • Hubei poty-like virus 1 is likely an interspecies recombinant of sugarcane mosaic virus and putative bean yellow mosaic virus

    • Ramamoorthy Sankaranarayanan
    • , Sankara Naynar Palani
    •  & Jebasingh Tennyson

    Archives of Virology (2019)

  • Taxonomy of the order Bunyavirales: second update 2018

    • Piet Maes
    • , Scott Adkins
    • , Sergey V. Alkhovsky
    • , Tatjana Avšič-Županc
    • , Matthew J. Ballinger
    • , Dennis A. Bente
    • , Martin Beer
    • , Éric Bergeron
    • , Carol D. Blair
    • , Thomas Briese
    • , Michael J. Buchmeier
    • , Felicity J. Burt
    • , Charles H. Calisher
    • , Rémi N. Charrel
    • , Il Ryong Choi
    • , J. Christopher S. Clegg
    • , Juan Carlos de la Torre
    • , Xavier de Lamballerie
    • , Joseph L. DeRisi
    • , Michele Digiaro
    • , Mike Drebot
    • , Hideki Ebihara
    • , Toufic Elbeaino
    • , Koray Ergünay
    • , Charles F. Fulhorst
    • , Aura R. Garrison
    • , George Fú Gāo
    • , Jean-Paul J. Gonzalez
    • , Martin H. Groschup
    • , Stephan Günther
    • , Anne-Lise Haenni
    • , Roy A. Hall
    • , Roger Hewson
    • , Holly R. Hughes
    • , Rakesh K. Jain
    • , Miranda Gilda Jonson
    • , Sandra Junglen
    • , Boris Klempa
    • , Jonas Klingström
    • , Richard Kormelink
    • , Amy J. Lambert
    • , Stanley A. Langevin
    • , Igor S. Lukashevich
    • , Marco Marklewitz
    • , Giovanni P. Martelli
    • , Nicole Mielke-Ehret
    • , Ali Mirazimi
    • , Hans-Peter Mühlbach
    • , Rayapati Naidu
    • , Márcio Roberto Teixeira Nunes
    • , Gustavo Palacios
    • , Anna Papa
    • , Janusz T. Pawęska
    • , Clarence J. Peters
    • , Alexander Plyusnin
    • , Sheli R. Radoshitzky
    • , Renato O. Resende
    • , Víctor Romanowski
    • , Amadou Alpha Sall
    • , Maria S. Salvato
    • , Takahide Sasaya
    • , Connie Schmaljohn
    • , Xiǎohóng Shí
    • , Yukio Shirako
    • , Peter Simmonds
    • , Manuela Sironi
    • , Jin-Won Song
    • , Jessica R. Spengler
    • , Mark D. Stenglein
    • , Robert B. Tesh
    • , Massimo Turina
    • , Tàiyún Wèi
    • , Anna E. Whitfield
    • , Shyi-Dong Yeh
    • , F. Murilo Zerbini
    • , Yong-Zhen Zhang
    • , Xueping Zhou
    •  & Jens H. Kuhn

    Archives of Virology (2019)

  • Identification and genetic analysis of Kadipiro virus isolated in Shandong province, China

    • Weijia Zhang
    • , Fan Li
    • , Aiguo Liu
    • , Xiaojuan Lin
    • , Shihong Fu
    • , Jingdong Song
    • , Guifang Liu
    • , Nan Shao
    • , Zexin Tao
    • , Qianying Wang
    • , Ying He
    • , Wenwen Lei
    • , Guodong Liang
    • , Aiqiang Xu
    • , Li Zhao
    •  & Huanyu Wang

    Virology Journal (2018)

  • Recent insights into the tick microbiome gained through next-generation sequencing

    • Telleasha L. Greay
    • , Alexander W. Gofton
    • , Andrea Paparini
    • , Una M. Ryan
    • , Charlotte L. Oskam
    •  & Peter J. Irwin

    Parasites & Vectors (2018)

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.