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Redefining the invertebrate RNA virosphere

Nature 540, 539–543 (22 December 2016) | Download Citation

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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.

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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

    • 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

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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

Extended data figures

  1. 1.

    The contribution of major viral clades to the total virome of each host phylum/order.

  2. 2.

    Phylogenetic incongruence between the RdRp and structural proteins.

  3. 3.

    The gain and loss of RNA virus structural proteins.

  4. 4.

    Lateral gene transfer between RNA viruses and cellular organisms.

Extended data tables

  1. 1.

    Distribution of homologous protein clusters across divergent taxonomic groups (RNA viruses, DNA viruses and cellular organisms)

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.

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About this article

Publication history

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DOI

https://doi.org/10.1038/nature20167

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