Light and Hydrogen Peroxide Inhibit C. elegans Feeding through Gustatory Receptor Orthologs and Pharyngeal Neurons

While gustatory sensing of the five primary flavors (sweet, salty, sour, bitter, and savory) has been extensively studied, pathways that detect non-canonical taste stimuli remain relatively unexplored. In particular, while reactive oxygen species cause generalized damage to biological systems, no gustatory mechanism to prevent ingestion of such material has been identified in any organism. We observed that light inhibits C. elegans feeding and used light as a tool to uncover molecular and neural mechanisms for gustation. Light can generate hydrogen peroxide, and we discovered that hydrogen peroxide similarly inhibits feeding. The gustatory receptor family members LITE-1 and GUR-3 are required for the inhibition of feeding by light and hydrogen peroxide. The I2 pharyngeal neurons increase calcium in response to light and hydrogen peroxide, and these responses require GUR-3 and a conserved antioxidant enzyme peroxiredoxin PRDX-2. Our results demonstrate a gustatory mechanism that mediates the detection and blocks ingestion of a non-canonical taste stimulus, hydrogen peroxide. •Light and hydrogen peroxide (H2O2) cause C. elegans to inhibit feeding and escape•Light and H2O2 are sensed via the gustatory receptor orthologs GUR-3 and LITE-1•The I2 pharyngeal neurons detect light and H2O2 via GUR-3 and peroxiredoxin PRDX-2•C. elegans light sensing likely occurs via generation of reactive oxygen species Is there more to taste than the five primary flavors? Bhatla et al. describe how C. elegans tastes and behaviorally responds to hydrogen peroxide. This sensing mechanism is also used to detect light, suggesting that light sensing in the worm relies on the tasting of reactive oxygen species.