Humidity sensation requires both mechanosensory and thermosensory pathways in Caenorhabditis elegans

Abstract

All terrestrial animals must find a proper level of moisture to ensure their health and survival. The cellular-molecular basis for sensing humidity is unknown in most animals, however. We used the model nematode Caenorhabditis elegans to uncover a mechanism for sensing humidity. We found that whereas C. elegans showed no obvious preference for humidity levels under standard culture conditions, worms displayed a strong preference after pairing starvation with different humidity levels, orienting to gradients as shallow as 0.03% relative humidity per millimeter. Cell-specific ablation and rescue experiments demonstrate that orientation to humidity in C. elegans requires the obligatory combination of distinct mechanosensitive and thermosensitive pathways. The mechanosensitive pathway requires a conserved DEG/ENaC/ ASIC mechanoreceptor complex in the FLP neuron pair. Because humidity levels influence the hydration of the worm's cuticle, our results suggest that FLP may convey humidity information by reporting the degree that subcuticular dendritic sensory branches of FLP neurons are stretched by hydration. The thermosensitive pathway requires cGMP-gated channels in the AFD neuron pair. Because humidity levels affect evaporative cooling, AFD may convey humidity information by reporting thermal flux. Thus, humidity sensation arises as a metamodality in C. elegans that requires the integration of parallel mechanosensory and thermosensory pathways. This hygrosensation strategy, first proposed by Thunberg more than 100 y ago, may be conserved because the underlying pathways have cellular and molecular equivalents across a wide range of species, including insects and humans. mechanosensation | thermosensation M oisture is essential for life. As such, many animals have adapted different behavioral mechanisms to migrate toward their preferred moisture level (hygrotaxis) (1-6). For instance, Drosophila avoid high humidity that impedes flight, whereas green frogs orient toward high humidity to maintain hydration (5, 6). Animals also sense moisture levels to determine important information about their environment; for example, moths detect humidity levels around flowers to deduce which ones might be damaged and contain less nectar (7). These behaviors are often critical to keep an animal within its niche and regulate essential processes such as growth and reproduction. Thus, it is surprising that the molecular basis for how different humidity levels are detected and encoded by the nervous system (hygrosensation) remains unknown in most animals.The search for humidity receptors has achieved the most progress in insects. For instance, distinct sets of hygrosensitive neurons have been found in dome-shaped organs on the antenna of the giant cockroach (8). One set activates with moist air, and the other set responds to dry air. Similar moist and dry receptive neurons have been detected in the branched arista subsegment of the antennae in adult Drosophila (9). Removal of the arista or deletion of any one of three TRP channels expres...

Humidity Sensing in Drosophila

“…Hygrosensation has previously been proposed to comprise a thermosensory component [5, 16]. Hence, we next set out to determine if IR21a, IR25a, IR93a and IR40a also mediate temperature responses.…”

Neurophysiology of Skin Thermal Sensations

“…In this respect, comparative results from animal studies exploring the molecular mechanisms of humidity sensation in hygroreceptor-lacking organisms (e.g. the roundworm Caenorhabditis elegans) (257), have shown some remarkable similarities in the hygrosensation strategies developed by humans and other animal species. These observations should be taken into account when considering the possibility to use animal models in combination with experiments in humans, as a way to further explore this area.…”

Multisensory integration in C. elegans

“…While a number of C. elegans sensory neurons are polymodal, many sensory neurons are often employed together to decode a complex sensory environment [24,27,34,46,59]. For example, carbon dioxide is a common sensory cue that may signal the presence of bacterial food sources to C. elegans.…”

“…Hygrosensation also requires integration of multiple sensory cues. Worms respond to humidity with FLP and AFD sensory neurons that are known to sense mechanical stimuli and temperature, respectively, to coordinate locomotory behaviors that drive hygrosensation [46]. Furthermore, even within the same sensory modality multiple sensory neurons are used to respond to complex cues.…”