Muscular expression of pezo-1 differentially influences swimming and crawling in C. elegans

Mechanosensitive PIEZO ion channels are evolutionarily conserved proteins that are widely expressed in neuronal and muscular tissues. This study explores the role of the mechanoreceptor PEZO-1 in the body wall muscles of Caenorhabditis elegans, focusing on its influence on two locomotor behaviors, swimming and crawling. Using confocal imaging, we reveal that PEZO-1 localizes to the sarcolemma and plays a crucial role in modulating calcium dynamics, which is important for muscle contraction. When we knocked down pezo-1 expression in striated muscles with RNA interference, calcium levels in head and tail muscles increased. However, we discovered differential effects on two locomotion modes displayed by C. elegans: while downregulation of pezo-1 led to an increase in crawling speed, the overall trajectory of the calcium signal during the crawl cycle remained the same. In contrast, pezo-1 downregulation caused a reduction in swimming speed, increased activation of the ventral tail muscles, and a disruption of dorsoventral movement asymmetry, a critical feature that enables propulsion in water. These alterations were correlated with impaired swimming posture and path curvature, suggesting that that PEZO-1 differentially modulates swimming and crawling behaviors.