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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

Francesco A. Servello, Rute Fernandes, Matthias Eder, Nathan Harris, Olivier M. F. Martin, Natasha Oswal, Anders Lindberg, Nohelly Derosiers, View ORCID ProfilePiali Sengupta, View ORCID ProfileNicholas Stroustrup, View ORCID ProfileJavier Apfeld
doi: https://doi.org/10.1101/2022.03.21.485202
Francesco A. Servello
1Biology Department, Northeastern University, Boston, Massachusetts, United States of America
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Rute Fernandes
2Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
3Universitat Pompeu Fabra (UPF), Barcelona, Spain
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Matthias Eder
2Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
3Universitat Pompeu Fabra (UPF), Barcelona, Spain
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Nathan Harris
4Department of Biology, Brandeis University, Waltham, MA, United States of America
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Olivier M. F. Martin
2Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
3Universitat Pompeu Fabra (UPF), Barcelona, Spain
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Natasha Oswal
2Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
3Universitat Pompeu Fabra (UPF), Barcelona, Spain
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Anders Lindberg
1Biology Department, Northeastern University, Boston, Massachusetts, United States of America
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Nohelly Derosiers
1Biology Department, Northeastern University, Boston, Massachusetts, United States of America
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Piali Sengupta
4Department of Biology, Brandeis University, Waltham, MA, United States of America
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  • ORCID record for Piali Sengupta
Nicholas Stroustrup
2Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain
3Universitat Pompeu Fabra (UPF), Barcelona, Spain
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Javier Apfeld
1Biology Department, Northeastern University, Boston, Massachusetts, United States of America
5Bioengineering Department, Northeastern University, Boston, Massachusetts, United States of America
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  • ORCID record for Javier Apfeld
  • For correspondence: j.apfeld@northeastern.edu
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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 strategy, which we call “enhancer sensing,” 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.

Competing Interest Statement

The authors have declared no competing interest.

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Posted March 23, 2022.
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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
Francesco A. Servello, Rute Fernandes, Matthias Eder, Nathan Harris, Olivier M. F. Martin, Natasha Oswal, Anders Lindberg, Nohelly Derosiers, Piali Sengupta, Nicholas Stroustrup, Javier Apfeld
bioRxiv 2022.03.21.485202; doi: https://doi.org/10.1101/2022.03.21.485202
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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
Francesco A. Servello, Rute Fernandes, Matthias Eder, Nathan Harris, Olivier M. F. Martin, Natasha Oswal, Anders Lindberg, Nohelly Derosiers, Piali Sengupta, Nicholas Stroustrup, Javier Apfeld
bioRxiv 2022.03.21.485202; doi: https://doi.org/10.1101/2022.03.21.485202

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