1. Microbiology and Infectious Disease
Download icon

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
Research Article
  • Cited 399
  • Views 10,412
  • Annotations
Cite this article as: eLife 2015;4:e05378 doi: 10.7554/eLife.05378

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

Publication 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

  • 10,412
    Page views
  • 2,159
    Downloads
  • 399
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, PubMed Central.

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)

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

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

  1. Further reading

Further reading

    1. Cell Biology
    2. Microbiology and Infectious Disease
    Yong Fu et al.
    Research Article

    Toxoplasma gondii has evolved different developmental stages for disseminating during acute infection (i.e. tachyzoites) and for establishing chronic infection (i.e. bradyzoites). Calcium ion (Ca2+) signaling tightly regulates the lytic cycle of tachyzoites by controlling microneme secretion and motility to drive egress and cell invasion. However, the roles of Ca2+ signaling pathways in bradyzoites remain largely unexplored. Here we show that Ca2+ responses are highly restricted in bradyzoites and that they fail to egress in response to agonists. Development of dual-reporter parasites revealed dampened Ca2+ responses and minimal microneme secretion by bradyzoites induced in vitro or harvested from infected mice and tested ex vivo. Ratiometric Ca2+ imaging demonstrated lower Ca2+ basal levels, reduced magnitude, and slower Ca2+ kinetics in bradyzoites compared with tachyzoites stimulated with agonists. Diminished responses in bradyzoites were associated with down-regulation of Ca2+-ATPases involved in intracellular Ca2+ storage in the endoplasmic reticulum (ER) and acidocalcisomes. Once liberated from cysts by trypsin digestion, bradyzoites incubated in glucose plus Ca2+ rapidly restored their intracellular Ca2+ and ATP stores leading to enhanced gliding. Collectively, our findings indicate that intracellular bradyzoites exhibit dampened Ca2+ signaling and lower energy levels that restrict egress, and yet upon release they rapidly respond to changes in the environment to regain motility.

    1. Microbiology and Infectious Disease
    Xiaotian Tang et al.
    Research Article Updated

    Adiponectin-mediated pathways contribute to mammalian homeostasis; however, little is known about adiponectin and adiponectin receptor signaling in arthropods. In this study, we demonstrate that Ixodes scapularis ticks have an adiponectin receptor-like protein (ISARL) but lack adiponectin, suggesting activation by alternative pathways. ISARL expression is significantly upregulated in the tick gut after Borrelia burgdorferi infection, suggesting that ISARL signaling may be co-opted by the Lyme disease agent. Consistent with this, RNA interference (RNAi)-mediated silencing of ISARL significantly reduced the B. burgdorferi burden in the tick. RNA-seq-based transcriptomics and RNAi assays demonstrate that ISARL-mediated phospholipid metabolism by phosphatidylserine synthase I is associated with B. burgdorferi survival. Furthermore, the tick complement C1q-like protein 3 interacts with ISARL, and B. burgdorferi facilitates this process. This study identifies a new tick metabolic pathway that is connected to the life cycle of the Lyme disease spirochete.