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.

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

  • 11,024
    views
  • 2,652
    downloads
  • 619
    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. Immunology and Inflammation
    2. Microbiology and Infectious Disease
    Benita Martin-Castaño, Patricia Diez-Echave ... Julio Galvez
    Research Article

    Coronavirus disease 2019 (COVID-19) is a respiratory illness caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) that displays great variability in clinical phenotype. Many factors have been described to be correlated with its severity, and microbiota could play a key role in the infection, progression, and outcome of the disease. SARS-CoV-2 infection has been associated with nasopharyngeal and gut dysbiosis and higher abundance of opportunistic pathogens. To identify new prognostic markers for the disease, a multicentre prospective observational cohort study was carried out in COVID-19 patients divided into three cohorts based on symptomatology: mild (n = 24), moderate (n = 51), and severe/critical (n = 31). Faecal and nasopharyngeal samples were taken, and the microbiota was analysed. Linear discriminant analysis identified Mycoplasma salivarium, Prevotella dentalis, and Haemophilus parainfluenzae as biomarkers of severe COVID-19 in nasopharyngeal microbiota, while Prevotella bivia and Prevotella timonensis were defined in faecal microbiota. Additionally, a connection between faecal and nasopharyngeal microbiota was identified, with a significant ratio between P. timonensis (faeces) and P. dentalis and M. salivarium (nasopharyngeal) abundances found in critically ill patients. This ratio could serve as a novel prognostic tool for identifying severe COVID-19 cases.

    1. Microbiology and Infectious Disease
    Vivian C Salgueiro-Toledo, Jorge Bertol ... Rafael Prados-Rosales
    Research Article

    Pathogenic and nonpathogenic mycobacteria secrete extracellular vesicles (EVs) under various conditions. EVs produced by Mycobacterium tuberculosis (Mtb) have raised significant interest for their potential in cell communication, nutrient acquisition, and immune evasion. However, the relevance of vesicle secretion during tuberculosis infection remains unknown due to the limited understanding of mycobacterial vesicle biogenesis. We have previously shown that a transposon mutant in the LCP-related gene virR (virRmut) manifested a strong attenuated phenotype during experimental macrophage and murine infections, concomitant to enhanced vesicle release. In this study, we aimed to understand the role of VirR in the vesicle production process in Mtb. We employ genetic, transcriptional, proteomics, ultrastructural, and biochemical methods to investigate the underlying processes explaining the enhanced vesiculogenesis phenomenon observed in the virRmut. Our results establish that VirR is critical to sustain proper cell permeability via regulation of cell envelope remodeling possibly through the interaction with similar cell envelope proteins, which control the link between peptidoglycan and arabinogalactan. These findings advance our understanding of mycobacterial extracellular vesicle biogenesis and suggest that these set of proteins could be attractive targets for therapeutic intervention.