1. Microbiology and Infectious Disease
  2. Neuroscience
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Thioredoxin shapes the C. elegans sensory response to Pseudomonas produced nitric oxide

  1. Yingsong Hao
  2. Wenxing Yang
  3. Jing Ren
  4. Qi Hall
  5. Yun Zhang  Is a corresponding author
  6. Joshua M Kaplan  Is a corresponding author
  1. Massachusetts General Hospital, United States
  2. Harvard University, United States
Research Article
  • Cited 9
  • Views 1,652
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Cite this article as: eLife 2018;7:e36833 doi: 10.7554/eLife.36833

Abstract

Nitric oxide (NO) is released into the air by NO-producing organisms; however, it is unclear if animals utilize NO as a sensory cue. We show that C. elegans avoids Pseudomonas aeruginosa (PA14) in part by detecting PA14-produced NO. PA14 mutants deficient for NO production fail to elicit avoidance and NO donors repel worms. PA14 and NO avoidance are mediated by a chemosensory neuron (ASJ) and these responses require receptor guanylate cyclases and cyclic nucleotide gated ion channels. ASJ exhibits calcium increases at both the onset and removal of NO. These NO-evoked ON and OFF calcium transients are affected by a redox sensing protein, TRX-1/thioredoxin. TRX-1's trans-nitrosylation activity inhibits the ON transient whereas TRX-1's de-nitrosylation activity promotes the OFF transient. Thus, C. elegans exploits bacterially produced NO as a cue to mediate avoidance and TRX-1 endows ASJ with a bi-phasic response to NO exposure.

Article and author information

Author details

  1. Yingsong Hao

    Department of Molecular Biology, Massachusetts General Hospital, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Wenxing Yang

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0965-787X
  3. Jing Ren

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Qi Hall

    Department of Molecular Biology, Massachusetts General Hospital, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Yun Zhang

    Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, United States
    For correspondence
    yzhang@oeb.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7631-858X
  6. Joshua M Kaplan

    Department of Molecular Biology, Massachusetts General Hospital, Boston, United States
    For correspondence
    kaplan@molbio.mgh.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7418-7179

Funding

National Institutes of Health (DK80215)

  • Joshua M Kaplan

National Institutes of Health (DC009852)

  • Yun Zhang

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Piali Sengupta, Brandeis University, United States

Publication history

  1. Received: March 21, 2018
  2. Accepted: July 1, 2018
  3. Accepted Manuscript published: July 17, 2018 (version 1)
  4. Version of Record published: July 30, 2018 (version 2)

Copyright

© 2018, Hao 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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