Neuronal temperature perception induces specific defenses that enable C. elegans to cope with the enhanced reactivity of hydrogen peroxide at high temperature
- Northeastern University, United States
- Centre for Genomic Regulation, Spain
- 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.
Article and author information
Author details
Nicholas Stroustrup
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
- Douglas Portman, University of Rochester, United States
Version history
- Preprint posted: March 23, 2022 (view preprint)
- Received: March 25, 2022
- Accepted: October 12, 2022
- Accepted Manuscript published: October 13, 2022 (version 1)
- 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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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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Geometric criteria can be used to assess whether cell intercalation is active or passive during the convergent extension of tissue.
