Opsins in the Cephalic and Extracephalic Photoreceptors in the Marine Gastropod Onchidium verruculatum

The marine gastropod Onchidium verruculatum has a pair of ocular photoreceptors, the stalk eyes, on the tip of its stalk near the head, as well as several extracephalic photosensory organs. The retinas of the stalk eye consist of two morphologically distinct visual cells, namely, the type I cells equipped with well-developed microvilli and the type II cells with less developed microvilli. The extracephalic photosensors comprise the dorsal eye, dermal photoreceptor, and brain photosensitive neurons. The characteristics of these cephalic and extracephalic photosensory organs have been studied from morphological and electrophysiological perspectives. However, little is known about the visual pigment molecules responsible for light detection in these organs. In the present study, we searched for opsin molecules that are expressed in the neural tissues of Onchidium and identified six putative signaling-competent opsin species, including Xenopsin1, Xenopsin2, Gq-coupled rhodopsin1, Gq-coupled rhodopsin2, Opsin-5B, and Gq-coupled rhodopsin-like. Immunohistochemical staining of four of the six opsins revealed that Xenopsin1, Gq-coupled rhodopsin1, and Gq-coupled rhodopsin2 are expressed in the rhabdomere of the stalk eye and in the dermal photoreceptor. Xenopsin2 was expressed in the type II photoreceptors of the stalk eye and in the ciliary photoreceptors of the dorsal eye. These immunohistochemical data were consistent with the results of the expression analysis, revealed by quantitative reverse transcription polymerase chain reaction. This study clarified the identities of opsins expressed in the extracephalic photosensory organs of Onchidium and the distinct molecular compositions among the photoreceptors.