A comparative molecular characterization of extraocular photoreceptors

Abstract

Extraocular photoreceptors exist across a wide range of taxa, and there is much interest in learning more about these types of photoreceptors. Many tissues, including the central nervous system, light organ, lateral line, genitalia, and skin, can contain photoreceptors utilized for a variety of tasks, such as regulation of circadian cycles, copulation, escape responses, and counterillumination. Many studies have focused on the presence of non-visual opsins that couple to phototransductive pathways different than those used for vision (e.g. melanopsin, pinopsin, parapinopsin). However, new evidence suggests that extraocular photoreceptors may also incorporate visual opsins and utilize phototransductive pathways typical of visual photoreceptors. In this dissertation, three animal phyla were used to contribute new knowledge concerning extraocular photoreceptors, including the presence of molecular components of visual phototransduction in extraocular tissues. Crustaceans, cephalopods, and fish represent a diverse sampling of animals that are hypothesized to have unique and undescribed extraocular photoreceptors that function using typical visual phototransduction pathways. Crayfish have a photoreceptor called the caudal photoreceptor, which initiates shadow-seeking behaviors as a means of concealment. This photoreceptor is located in the sixth abdominal ganglion of the ventral nerve cord and is hypothesized to function using an opsin based visual pigment. I found two opsin transcripts in the retina and in each ganglion of the central nervous system, including the sixth abdominal ganglion in the red swamp crayfish, Procambarus clarkii. The long-wavelength sensitive (LWS) opsin protein, expressed in the main rhabdoms of the retina and the short-wavelength sensitive (SWS) opsin, expressed in the R8 cells distal to the main rhabdoms, are also expressed in small nerve fibers in the cerebral ganglion and throughout the ventral nerve cord, including the sixth abdominal ganglion. The presence of opsin transcripts and proteins throughout the central nervous system suggests that the caudal photoreceptor could function using visual opsins and a visual phototransduction pathway, but also that unidentified photoreceptors exist throughout the central nervous system. Cephalopods use chromatophores for camouflage and signaling. Interestingly, rhodopsin, retinochrome, Gq?, and squid transient receptor potential channel gene transcripts were discovered in my research in skin and muscle tissues of the squid Doryteuthis pealeii and the cuttlefishes Sepia officinalis and Sepia latimanus. In fact, rhodopsin, retinochrome, and Gq? proteins are expressed in specific regions of chromatophore organs that are used for camouflage and signaling in D. pealeii including the pigment sacs, radial muscle fibers, and sheath cells. Furthermore, D. pealeii fin muscle, hair cells, axial ganglia, and peduncle nerves express rhodopsin and retinochrome proteins, which suggest the presence of photoreceptors in many tissues throughout their bodies. Similar to cephalopods, flat fish (including the summer flounder, Paralichthys dentatus) are known to use dynamic patterning to achieve camouflage and signaling. Some fish chromatophores can contain photoreceptors, but fish that use dynamic patterning have not yet been investigated. Five visual opsin transcripts were identified in dermal tissues from all regions of the body of P. dentatus, all identical to those expressed in the retina. Additionally, one melanopsin transcript identical to a melanopsin transcript found in the retina is located in the ventral skin, dorsal fin, and caudal fin. Interestingly, the five visual opsins, when expressed in the retina, are expressed in photoreceptors that detect light for image formation. Conversely, melanopsin is a well-described non-visual retinal opsin that is expressed in photoreceptors that are primarily involved in non-image forming vision. Given these results, it is possible that flounders have dermal photoreceptors in their chromatophores that utilize visual and non-visual opsins, and that these photoreceptors may play a role in dynamic patterning in the dermis of these animals. Collectively these results suggest that visual opsins and visual phototransduction components are commonly utilized in extraocular photoreceptors across a wide range of animals. This research also suggests that many animals have extraocular photoreceptors that are unidentified and require greater attention to learn about the molecular, physiological, and functional characteristics of such photoreceptive systems.