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

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. Author summaryOne of the most common lethal threats that nematodes encounter is hydrogen peroxide, which is produced by a wide variety of microorganisms. In this microbial battlefield, how do nematodes find a niche that provides the food and safety necessary for growth and reproduction? In the present study, we developed a model ecosystem to study the behavioral mechanisms that enable the nematode C. elegans to find those niches. We found that C. elegans adjust their behavior to find bacterial communities that provide protection from hydrogen peroxide. Hydrogen peroxide and bacteria had opposing effects on the activity of sensory neurons that modulate the nematode's locomotion towards bacteria and away from hydrogen peroxide. The diminished perception of bacteria unable to degrade hydrogen peroxide in the environment represents a general mechanism enabling nematodes to leave environments where the bacterial community does not provide them and their future progeny with sufficient protection from hydrogen peroxide.