Intestinal infection regulates behavior and learning via neuroendocrine signaling

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Abstract

The recognition of pathogens and subsequent activation of defense responses are critical for the survival of organisms. The nematode Caenorhabditis elegans recognizes pathogenic bacteria and elicits defense responses by activating immune pathways and pathogen avoidance. Here we show that chemosensation of phenazines produced by pathogenic Pseudomonas aeruginosa, which leads to rapid activation of DAF-7/TGF-β in ASJ neurons, is insufficient for the elicitation of pathogen avoidance behavior. Instead, intestinal infection and bloating of the lumen, which depend on the virulence of P. aeruginosa, regulates both pathogen avoidance and aversive learning by modulating not only the DAF-7/TGF-β pathway but also the G-protein coupled receptor NPR-1 pathway, which also controls aerotaxis behavior. Modulation of these neuroendocrine pathways by intestinal infection serves as a systemic feedback that enables animals to avoid virulent bacteria. These results reveal how feedback from the intestine during infection can modulate the behavior, learning, and microbial perception of the host.

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

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Jogender Singh

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 Institute of General Medical Sciences (GM0709077)

Alejandro Aballay

National Institute of Allergy and Infectious Diseases (AI117911)

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.