Anoctamins mediate polymodal sensory perception and larval metamorphosis in a non-vertebrate chordate.

Abstract

An exceptional feature of most animals is their ability to perceive diverse sensory cues from the environment and integrate this information in their brain to yield ethologically relevant behavioral output. For the myriad of marine species, the ocean represents a complex sensory environment, which acts as a crucible of evolution for polymodal sensory perception. The cellular and molecular bases of polymodal sensory perception in a marine environment remain enigmatic. Here we use Ca2+ imaging and quantitative behavioral analysis to show that in the tunicate Ciona intestinalis two members of the evolutionarily conserved Anoctamin family1-4 (Tmem16E/Ano5 and Tmem16F/Ano6), are required for sensing chemosensory and mechanosensory metamorphic cues. We find that they act by modulating neuronal excitability and Ca2+ response kinetics in the primary sensory neurons and axial columnar cells of the papillae, a widely conserved sensory-adhesive organ across ascidians5-9. Finally, we use electrophysiological recordings and a scramblase assay in tissue culture to demonstrate that Tmem16E/Ano5 acts as a channel, while Tmem16F/Ano6 is a bifunctional ion channel and phospholipid scramblase. Our results establish Ano5 and Ano6 as novel players in the zooplanktonic, pre-vertebrate molecular toolkit that controls polymodal sensory perception in aquatic environments.