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.

Metrics

  • 10,905
    views
  • 2,589
    downloads
  • 589
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.05378

Further reading

    1. Epidemiology and Global Health
    2. Microbiology and Infectious Disease
    Patrick E Brown, Sze Hang Fu ... Ab-C Study Collaborators
    Research Article Updated

    Background:

    Few national-level studies have evaluated the impact of ‘hybrid’ immunity (vaccination coupled with recovery from infection) from the Omicron variants of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2).

    Methods:

    From May 2020 to December 2022, we conducted serial assessments (each of ~4000–9000 adults) examining SARS-CoV-2 antibodies within a mostly representative Canadian cohort drawn from a national online polling platform. Adults, most of whom were vaccinated, reported viral test-confirmed infections and mailed self-collected dried blood spots (DBSs) to a central lab. Samples underwent highly sensitive and specific antibody assays to spike and nucleocapsid protein antigens, the latter triggered only by infection. We estimated cumulative SARS-CoV-2 incidence prior to the Omicron period and during the BA.1/1.1 and BA.2/5 waves. We assessed changes in antibody levels and in age-specific active immunity levels.

    Results:

    Spike levels were higher in infected than in uninfected adults, regardless of vaccination doses. Among adults vaccinated at least thrice and infected more than 6 months earlier, spike levels fell notably and continuously for the 9-month post-vaccination. In contrast, among adults infected within 6 months, spike levels declined gradually. Declines were similar by sex, age group, and ethnicity. Recent vaccination attenuated declines in spike levels from older infections. In a convenience sample, spike antibody and cellular responses were correlated. Near the end of 2022, about 35% of adults above age 60 had their last vaccine dose more than 6 months ago, and about 25% remained uninfected. The cumulative incidence of SARS-CoV-2 infection rose from 13% (95% confidence interval 11–14%) before omicron to 78% (76–80%) by December 2022, equating to 25 million infected adults cumulatively. However, the coronavirus disease 2019 (COVID-19) weekly death rate during the BA.2/5 waves was less than half of that during the BA.1/1.1 wave, implying a protective role for hybrid immunity.

    Conclusions:

    Strategies to maintain population-level hybrid immunity require up-to-date vaccination coverage, including among those recovering from infection. Population-based, self-collected DBSs are a practicable biological surveillance platform.

    Funding:

    Funding was provided by the COVID-19 Immunity Task Force, Canadian Institutes of Health Research, Pfizer Global Medical Grants, and St. Michael’s Hospital Foundation. PJ and ACG are funded by the Canada Research Chairs Program.

    1. Microbiology and Infectious Disease
    Alejandro Prieto, Luïsa Miró ... Antonio Juarez
    Research Article

    Antimicrobial resistance (AMR) poses a significant threat to human health. Although vaccines have been developed to combat AMR, it has proven challenging to associate specific vaccine antigens with AMR. Bacterial plasmids play a crucial role in the transmission of AMR. Our recent research has identified a group of bacterial plasmids (specifically, IncHI plasmids) that encode large molecular mass proteins containing bacterial immunoglobulin-like domains. These proteins are found on the external surface of the bacterial cells, such as in the flagella or conjugative pili. In this study, we show that these proteins are antigenic and can protect mice from infection caused by an AMR Salmonella strain harboring one of these plasmids. Furthermore, we successfully generated nanobodies targeting these proteins, that were shown to interfere with the conjugative transfer of IncHI plasmids. Considering that these proteins are also encoded in other groups of plasmids, such as IncA/C and IncP2, targeting them could be a valuable strategy in combating AMR infections caused by bacteria harboring different groups of AMR plasmids. Since the selected antigens are directly linked to AMR itself, the protective effect extends beyond specific microorganisms to include all those carrying the corresponding resistance plasmids.