The mechanosensory DEG/ENaC channel DEGT-1 is a proprioceptor of C. elegans foregut movement

Abstract

The gastrointestinal tract is subjected to extensive mechanosensory stimulation during food ingestion. However, the identities of mechanosensory receptors in the enteric nervous system are largely unknown. The pharynx of C. elegans is a structurally and functionally homologous model of the vertebrate foregut, but is comprised of only 20 neurons that are embedded within the muscles and epithelial cells of the organ. Here we report that the DEG/ENaC family ion channel DEGT-1 is a proprioceptor of pharynx movement. DEGT-1 protein is expressed in 4 pharyngeal neurons (MI, M3, I4, and M5) and localized to their neuronal soma in direct contact with the collagenous pharyngeal basement membrane. degt-1 mutants display abnormally rapid feeding in the presence of food, causing global changes in lipid accumulation. degt-1 mutants also pump rapidly when pumping is induced by the presence of serotonin alone, suggesting that DEGT-1 is required for proprioception of pharyngeal pumping itself, rather than sensing ingested food. DEGT-1 is required in only two pharyngeal neurons (I4 and M5) to control pumping rate. Taken together, these results suggest that DEGT-1 modulates pharyngeal pumping rate by relaying proprioceptive feedback generated by the shear force of the pharynx against its own basement membrane. Thus, mechanosensors in enteric nervous systems modulate organ function not only by detecting forces from ingested contents, but also the movements of the organ itself.