TRPM channels mediate learned pathogen avoidance following intestinal distention

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Abstract

Upon exposure to harmful microorganisms, hosts engage in protective molecular and behavioral immune responses, both of which are ultimately regulated by the nervous system. Using the nematode Caenorhabditis elegans, we show that ingestion of E. faecalis leads to a fast pathogen avoidance behavior that results in aversive learning. We have identified multiple sensory mechanisms involved in the regulation of avoidance of E. faecalis. The G-protein coupled receptor NPR-1-dependent oxygen-sensing pathway opposes this avoidance behavior, while an ASE neuron-dependent pathway and an AWB and AWC neuron-dependent pathway are directly required for avoidance. Colonization of the anterior part of the intestine by E. faecalis leads to AWB and AWC mediated olfactory aversive learning. Finally, two transient receptor potential melastatin (TRPM) channels, GON-2 and GTL-2, mediate this newly described rapid pathogen avoidance. These results suggest a mechanism by which TRPM channels may sense the intestinal distension caused by bacterial colonization to elicit pathogen avoidance and aversive learning by detecting changes in host physiology.

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All data generated or analyzed during this study are included in the manuscript and supporting files.

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Adam Filipowicz

Department of Molecular Microbiology and Immunology, Oregon Health and Science University, Portland, United States

Competing interests
The authors declare that no competing interests exist.
Jonathan Lalsiamthara

Department of Molecular Microbiology and Immunology, Oregon Health and Science University, Portland, United States

Competing interests
The authors declare that no competing interests exist.
Alejandro Aballay

Department of Molecular Microbiology and Immunology, Oregon Health and Science University, Portland, United States

For correspondence
aballay@ohsu.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-5975-3352

Funding

National Institutes of Health (GM070907)

Alejandro Aballay

National Institutes of Health (AI156900)

Alejandro Aballay

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

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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.