Phototaxis and Phototransduction Mechanisms in the Model System C. elegans.

Abstract

C. elegans has become an increasingly popular model system for the study of sensory systems, in particular olfactory transduction and mechanotransduction. However, C. elegans is eyeless and lives in darkness (i.e. soil), and this organism has generally been presumed to be photoinsensitive. The ability to sense light is crucial to the survival of many organisms. In my thesis work I challenged the assumption that C. elegans is photoinsensitive, reasoning that light might serve functions other than “vision” per se. For instance, negative phototaxis behavior in C. elegans could function to retain worms in soil, or protect them from harmful effects of UV light. In my thesis research, I found that light stimuli, indeed, elicit avoidance behavior in C. elegans, and that prolonged light stimulation is lethal to worms. We also identified a group of ciliary sensory neurons as candidate photoreceptor cells. In a subset of these neurons (ASJ and ASK), we showed that light evokes a depolarizing conductance mediated by cyclic guanosine monophosphate (cGMP)-sensitive cyclic nucleotide-gated (CNG) channels.

By recording the photoreceptor neuron ASJ and ASK in wild-type and various mutant worms, we found that phototransduction is a G protein–mediated process and requires membrane-associated guanylate cyclases, but not typical phosphodiesterases. In addition, we found that C. elegans phototransduction requires LITE-1, a candidate photoreceptor protein known to be a member of the invertebrate taste receptor family. Our genetic, pharmacological and electrophysiological data suggest a model in which LITE-1 transduces light signals via G protein signaling, which leads to upregulation of the second messenger cGMP, followed by opening of cGMP-sensitive CNG channels and stimulation of photoreceptor cells. Our results identify a phototransduction cascade in C. elegans and implicate the function of a ‘taste receptor’ in phototransduction.