Environmental osmolarity presents a common type of sensory stimuli to animals. While behavioral responses to osmotic changes are important for maintaining a stable intracellular osmolarity, the underlying mechanisms are not fully understood. In the natural habitat of C. elegans, changes in environmental osmolarity are commonplace. It is known that the nematode acutely avoids shocks of extremely high osmolarity. Here, we show that C. elegans also generates gradually increased aversion of mild upshifts in environmental osmolarity. Different from an acute avoidance of osmotic shocks that depends on the function of a TRPV channel, the slow aversion to osmotic upshifts requires the cGMP-gated sensory channel subunit TAX-2. TAX-2 acts in several sensory neurons that are exposed to the body fluid to generate the aversive response through a motor network that underlies navigation. Osmotic upshifts activate the body cavity sensory neuron URX, which is known to induce aversion upon activation. Together, our results characterize the molecular and cellular mechanisms underlying a novel sensorimotor response to osmotic stimuli and reveal that C. elegans engages different behaviors and the underlying mechanisms to regulate responses to extracellular osmolarity.
Significance Statement Extracellular osmolarity presents an ecologicalal factor essential for the survival of all organisms. However, how animals respond to environmental osmolarity is not fully understood. We show that C. elegans responds to the upshifts of extracellular osmolarity by gradually increasing reorienting movements and the aversive response requires a conserved cGMP-gated channel subunit TAX-2. TAX-2 acts in several neurons that are exposed to the body fluid to regulate the response to osmotic upshifts. This behavior employs different channels and sensory neurons from a previously characterized acute avoidance of osmotic shocks, which is mediated by a TRPV channel in a sensory neuron open to the outside. Thus, our results reveal a novel sensorimotor response to extracellular osmolarity and the underlying mechanisms.
Authors report no conflict of interest.