Extraocular, rod-like photoreceptors in a flatworm express xenopsin photopigment

Animals detect light using opsin photopigments. One recently classified opsin clade, the xenopsins, found in lophotrochozoans, challenges our views on opsin and photoreceptor evolution. Originally thought to belong to the Gi-coupled ciliary opsins, xenopsins are now understood to have diverged from ciliary opsins in pre-bilaterian times, but little is known about the cells that deploy these proteins, or if they form a photopigment and drive phototransduction. We characterized xenopsin in a flatworm, Maritigrella crozieri, and found that it is expressed in a larval eyespot, and in an abundant extraocular cell type around the adult brain. These distinct cells house hundreds of cilia in an intra-cellular vacuole (a phaosome). Cellular assays show Mc xenopsin forms a photopigment and couples to Gi/o in response to light. These findings reveal a novel photoreceptor cell type and opsin/G-protein couple, and highlight the convergent enclosure of photosensitive cilia in flatworm phaosomes and jawed vertebrate rods.