Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses

  1. Ci-Xiu Li
  2. Mang Shi
  3. Jun-Hua Tian
  4. Xian-Dan Lin
  5. Yan-Jun Kang
  6. Liang-Jun Chen
  7. Xin-Cheng Qin
  8. Jianguo Xu
  9. Edward C Holmes
  10. Yong-Zhen Zhang  Is a corresponding author
  1. National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, China
  2. Wuhan Center for Disease Control and Prevention, China
  3. Wenzhou Center for Disease Control and Prevention, China

Abstract

Although arthropods are important viral vectors, the biodiversity of arthropod viruses, as well as the role that arthropods have played in viral origins and evolution, is unclear. Through RNA sequencing of 70 arthropod species we discovered 112 novel viruses that appear to be ancestral to much of the documented genetic diversity of negative-sense RNA viruses, a number of which are also present as endogenous genomic copies. With this greatly enriched diversity we revealed that arthropods contain viruses that fall basal to major virus groups, including the vertebrate-specific arenaviruses, filoviruses, hantaviruses, influenza viruses, lyssaviruses, and paramyxoviruses. We similarly documented a remarkable diversity of genome structures in arthropod viruses, including a putative circular form, that sheds new light on the evolution of genome organization. Hence, arthropods are a major reservoir of viral genetic diversity and have likely been central to viral evolution.

Article and author information

Author details

  1. Ci-Xiu Li

    State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Mang Shi

    State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Jun-Hua Tian

    Wuhan Center for Disease Control and Prevention, Wuhan, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Xian-Dan Lin

    Wenzhou Center for Disease Control and Prevention, Wenzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Yan-Jun Kang

    State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Liang-Jun Chen

    State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Xin-Cheng Qin

    State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Jianguo Xu

    State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Edward C Holmes

    State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Yong-Zhen Zhang

    State Key Laboratory for Infectious Disease Prevention and Control, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China
    For correspondence
    zhangyongzhen@icdc.cn
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Stephen P Goff, Howard Hughes Medical Institute, Columbia University, United States

Version history

  1. Received: October 29, 2014
  2. Accepted: January 27, 2015
  3. Accepted Manuscript published: January 29, 2015 (version 1)
  4. Version of Record published: March 9, 2015 (version 2)

Copyright

© 2015, Li et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Ci-Xiu Li
  2. Mang Shi
  3. Jun-Hua Tian
  4. Xian-Dan Lin
  5. Yan-Jun Kang
  6. Liang-Jun Chen
  7. Xin-Cheng Qin
  8. Jianguo Xu
  9. Edward C Holmes
  10. Yong-Zhen Zhang
(2015)
Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses
eLife 4:e05378.
https://doi.org/10.7554/eLife.05378

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