Modulation of sensory perception by hydrogen peroxide enables Caenorhabditis elegans to find a niche that provides both food and protection from hydrogen peroxide

PLoS Pathog. 2021 Dec 23;17(12):e1010112. doi: 10.1371/journal.ppat.1010112. eCollection 2021 Dec.

Abstract

Hydrogen peroxide (H2O2) is the most common chemical threat that organisms face. Here, we show that H2O2 alters the bacterial food preference of Caenorhabditis elegans, enabling the nematodes to find a safe environment with food. H2O2 induces the nematodes to leave food patches of laboratory and microbiome bacteria when those bacterial communities have insufficient H2O2-degrading capacity. The nematode's behavior is directed by H2O2-sensing neurons that promote escape from H2O2 and by bacteria-sensing neurons that promote attraction to bacteria. However, the input for H2O2-sensing neurons is removed by bacterial H2O2-degrading enzymes and the bacteria-sensing neurons' perception of bacteria is prevented by H2O2. The resulting cross-attenuation provides a general mechanism that ensures the nematode's behavior is faithful to the lethal threat of hydrogen peroxide, increasing the nematode's chances of finding a niche that provides both food and protection from hydrogen peroxide.

Grant support

This work was funded by a National Science Foundation CAREER grant #1750065 to J.A., a Burroughs Wellcome Fund award to V.V., an American Federation for Aging Research award to V.V., a National Institutes of Health grant DP2DK116645 to B.S.S., a Department of Energy Joint Genome Institute grant CSP503338 to B.S.S., a National Science Foundation Research Experiences for Undergraduates Award #1757443 to O.B., and a Northeastern University Tier 1 award to V.V. and J.A. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.