Chemosensory signal transduction inCaenorhabditis elegans

Abstract

Chemosensory neurons translate perception of external chemical cues, including odorants, tastants, and pheromones, into information that drives attraction or avoidance motor programs. In the laboratory, robust behavioral assays, coupled with powerful genetic, molecular and optical tools, have made Caenorhabditis elegans an ideal experimental system in which to dissect the contributions of individual genes and neurons to ethologically relevant chemosensory behaviors. Here, we review current knowledge of the neurons, signal transduction molecules and regulatory mechanisms that underlie the response of C. elegans to chemicals, including pheromones. The majority of identified molecules and pathways share remarkable homology with sensory mechanisms in other organisms. With the development of new tools and technologies, we anticipate that continued study of chemosensory signal transduction and processing in C. elegans will yield additional new insights into the mechanisms by which this animal is able to detect and discriminate among thousands of chemical cues with a limited sensory neuron repertoire.

Context-dependent inversion of the response in a single sensory neuron type reverses olfactory preference behavior

“…A potential advantage of differential usage of intracellular signaling pathways over modulation of sensory neuron synaptic output is the ability to discriminate between, and differentially respond to, each stimulus sensed by that neuron in a context-dependent manner. This mechanism is particularly advantageous for polymodal sensory neurons such as those in C. elegans (Ferkey et al, 2021) in which state-dependent engagement of different signaling pathways within a single sensory neuron type may allow animals to more effectively assess the salience of individual olfactory cues. Complex chemical response strategies have also been described in Drosophila gustatory neurons that express multiple ligand-gated ion channel receptors for different chemicals, and may represent a general mechanism by which organisms efficiently encode stimulus properties (Devineni et al, 2021;Stanley et al, 2021).…”

“…To probe the molecular mechanisms underlying the context-mediated hexanol response inversion in AWC, we tested the behaviors and hexanol responses of mutants previously implicated in AWC sensory signal transduction. Binding of odorants to their cognate receptors in AWC decreases intracellular cGMP levels either via inhibiting the activity of receptor guanylyl cyclases such as ODR-1 and DAF-11, and/or by promoting the activity of one or more phosphodiesterases, via heterotrimeric G proteins (Figure 3A) (Ferkey et al, 2021). Reduced intracellular cGMP levels closes cGMP-gated channels, inhibits calcium influx, and promotes attraction (Figure 3A) (Chalasani et al, 2007;Ferkey et al, 2021).…”

“…The copyright holder for this preprint this version posted November 9, 2021. ; https://doi.org/10.1101/2021.11.08.467792 doi: bioRxiv preprint chemicals (Bargmann et al, 1993;Ferkey et al, 2021). Each chemosensory neuron type in C. elegans expresses multiple chemoreceptors that are likely tuned to different odorants, a subset of which can be behaviorally discriminated (Troemel et al, 1995;Vidal et al, 2018).…”

“…elegans senses and navigates its complex chemical environment using a small subset of sensory neurons (Perkins et al, 1986;Ward et al, 1975;White et al, 1986). The valence of individual chemicals is largely determined by the responding sensory neuron type, such that distinct subsets of chemosensory neurons drive either attraction or avoidance to different chemicals (Bargmann et al, 1993;Ferkey et al, 2021). Each chemosensory neuron type in C. elegans expresses multiple chemoreceptors that are likely tuned to different odorants, a subset of which can be behaviorally discriminated (Troemel et al, 1995;Vidal et al, 2018).…”

Modulation of sensory perception by hydrogen peroxide enables Caenorhabditis elegans to find a niche that provides both food and protection from hydrogen peroxide

“…How did C. elegans overcome its strong attraction towards E. coli to specifically leave lawns that did not degrade hydrogen peroxide? C. elegans relies on sensory perception of bacterially derived cues to efficiently find the bacteria it feeds on (Ferkey et al, 2021). Most sensory functions in C. elegans hermaphrodites are performed by 60 ciliated and 12 non-ciliated neurons (White et al, 1986).…”