Muscular expression of pezo-1 differentially contributes to swimming and crawling production in the nematode 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 that are 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. While heightened, the overall trajectory of the calcium signal during the crawl cycle remained the same. While downregulation of pezo-1 led to an increase in crawling speed, it caused a reduction in swimming speed. Reduction in pezo-1 expression also resulted in the 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 PEZO-1 has different functions during swimming and crawling.

The mechanoreceptor pezo-1 is required for normal crawling locomotion in the nematode C. elegans.

The discovery in 2010 of the PIEZO family of mechanoreceptors revolutionized our understanding of the role of proprioceptive feedback in mammalian physiology. Much remains to be elucidated. This study looks at the role this receptor plays in normal locomotion. Like humans, the nematode C. elegans expresses PIEZO-type channels (encoded by the pezo-1 gene) throughout its somatic musculature. Here we use the unbiased automated behavioral software Tierpsy to characterize the effects that mutations removing PEZO-1 from body wall musculature have on C. elegans crawling. We find that loss of PEZO-1 results in disrupted locomotion and posture, consistent with phenotypes associated with loss of PIEZO2 in human musculature. C. elegans is thus an amenable system to study the role of mechanoreception on muscle physiology and function.