Neuronal temperature perception induces specific defenses that enable C. elegans to cope with the enhanced reactivity of hydrogen peroxide at high temperature

  1. Francesco A Servello
  2. Rute Fernandes
  3. Matthias Eder
  4. Nathan Harris
  5. Olivier M F Martin
  6. Natasha Oswal
  7. Anders Lindberg
  8. Nohelly Derosiers
  9. Piali Sengupta
  10. Nicholas Stroustrup
  11. Javier Apfeld  Is a corresponding author
  1. Northeastern University, United States
  2. Centre for Genomic Regulation, Spain
  3. Brandeis University, United States

Abstract

Hydrogen peroxide is the most common reactive chemical that organisms face on the microbial battlefield. The rate with which hydrogen peroxide damages biomolecules required for life increases with temperature, yet little is known about how organisms cope with this temperature-dependent threat. Here, we show that Caenorhabditis elegans nematodes use temperature information perceived by sensory neurons to cope with the temperature-dependent threat of hydrogen peroxide produced by the pathogenic bacterium Enterococcus faecium. These nematodes preemptively induce the expression of specific hydrogen peroxide defenses in response to perception of high temperature by a pair of sensory neurons. These neurons communicate temperature information to target tissues expressing those defenses via an insulin/IGF1 hormone. This is the first example of a multicellular organism inducing their defenses to a chemical when they sense an inherent enhancer of the reactivity of that chemical.

Data availability

Raw mRNA-seq read files are available under Bioproject PRJNA822361 (https://www.ncbi.nlm.nih.gov/bioproject/PRJNA822361).All data generated or analyzed during this study are included in the manuscript and supporting files.

The following data sets were generated

Article and author information

Author details

  1. Francesco A Servello

    Biology Department, Northeastern University, Boston, United States
    Competing interests
    No competing interests declared.
  2. Rute Fernandes

    Systems Biology Programme, Centre for Genomic Regulation, Barcelona, Spain
    Competing interests
    No competing interests declared.
  3. Matthias Eder

    Systems Biology Programme, Centre for Genomic Regulation, Barcelona, Spain
    Competing interests
    No competing interests declared.
  4. Nathan Harris

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7856-520X
  5. Olivier M F Martin

    Systems Biology Programme, Centre for Genomic Regulation, Barcelona, Spain
    Competing interests
    No competing interests declared.
  6. Natasha Oswal

    Systems Biology Programme, Centre for Genomic Regulation, Barcelona, Spain
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1478-8356
  7. Anders Lindberg

    Biology Department, Northeastern University, Boston, United States
    Competing interests
    No competing interests declared.
  8. Nohelly Derosiers

    Biology Department, Northeastern University, Boston, United States
    Competing interests
    No competing interests declared.
  9. Piali Sengupta

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    Piali Sengupta, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7468-0035
  10. Nicholas Stroustrup

    Systems Biology Programme, Centre for Genomic Regulation, Barcelona, Spain
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9530-7301
  11. Javier Apfeld

    Biology Department,, Northeastern University, Boston, United States
    For correspondence
    j.apfeld@northeastern.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9897-5671

Funding

National Science Foundation (CAREER 1750065)

  • Javier Apfeld

The Spanish Ministry of Economy, Industry and Competitiveness MEIC Excelencia award (PID2020-115189GB-I00)

  • Nicholas Stroustrup

Northeastern University (Tier 1)

  • Javier Apfeld

CERCA Programme/Generalitat de Catalunya

  • Nicholas Stroustrup

The Centro de Excelencia Severo Ochoa (CEX2020-001049-S,MCIN/AEI /10.13039/501100011033)

  • Nicholas Stroustrup

European Research Council (852201)

  • Nicholas Stroustrup

National Institutes of Health (R35 GM122463)

  • Piali Sengupta

National Institutes of Health (F32 NS112453)

  • Nathan Harris

National Science Foundation (1757443)

  • Nohelly Derosiers

The Spanish Ministry of the Economy, Industry and Competitiveness to the EMBL partnership

  • Nicholas Stroustrup

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

Reviewing Editor

  1. Douglas Portman, University of Rochester, United States

Publication history

  1. Preprint posted: March 23, 2022 (view preprint)
  2. Received: March 25, 2022
  3. Accepted: October 12, 2022
  4. Accepted Manuscript published: October 13, 2022 (version 1)
  5. Version of Record published: November 4, 2022 (version 2)

Copyright

© 2022, Servello 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. Francesco A Servello
  2. Rute Fernandes
  3. Matthias Eder
  4. Nathan Harris
  5. Olivier M F Martin
  6. Natasha Oswal
  7. Anders Lindberg
  8. Nohelly Derosiers
  9. Piali Sengupta
  10. Nicholas Stroustrup
  11. Javier Apfeld
(2022)
Neuronal temperature perception induces specific defenses that enable C. elegans to cope with the enhanced reactivity of hydrogen peroxide at high temperature
eLife 11:e78941.
https://doi.org/10.7554/eLife.78941
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