Opsin-based photoreception in Crinoids

Abstract

Opsin-mediated light perception has been investigated in many marine invertebrates including some clades of echinoderms such as sea stars, sea urchins and brittle stars. On the other hand, the understanding of potential light perception in crinoids, the basal lineage of the echinoderm phylum, remains largely unexplored. Only a few behavioural observations suggest that crinoids may be sensitive to light stimuli. This study investigates the behavioural and molecular basis of opsin-based photoreception in Antedon bifida, a European crinoid species belonging to the Comatulid order. In this context, the behavioural response to different light wavelengths, the characterisation of opsin genes in the recent chromosome-scale genome of this species and the opsin immunolocalisation within the crinoid tissues have been investigated. Behavioural tests pointed to a significant negative phototactic behaviour induced by a wide range of light wavelengths (463 to 630 nm) with maximum sensitivity to blue light (λmax = 463 nm). In silico genome analyses revealed the presence of only three rhabdomeric opsin genes located on chromosomes 4 and 6: Abif-opsins 4.1, 4.2 and 4.3. All crinoid opsins are phylogenetically clustered as a sister-group of all other echinoderm rhabdomeric opsins, supporting their evolution via duplication of an ancestral gene in the crinoid lineage. The low opsin diversity contrasts with other echinoderms which are generally characterised by up to eight bilaterian opsin groups. Interestingly, A. bifida opsin sequences present typical amino acid residues of rhabdomeric opsins of other bilaterians, including two conserved cysteines (C110, C187), the probable ancestral E181 counterion, a NPxxY(x)6F pattern, a highly conserved lysine potentially covalently bound to a chromophore, and the (D)RY motif, all supportive of photoreceptive functions. Finally, immunoreactivity to newly generated antibodies designed against sea star opsins was highlighted in several tissues associated with the ambulacral grooves of the calyx and the pinnules. Within these tissues, Abif-opsins (potentially the Abif-opsin 4.1) are expressed in the ectoneural basiepithelial nerve plexus and the hyponeural nerve plexus. On the other hand, a different opsin type (potentially the Abif-opsin 4.2) is also expressed in the sensory papillae of tube feet. The localization of at least two opsin types in different sensory structures suggests the presence of a complex extraocular photoreception system exclusively based on rhabdomeric opsins in this crinoid species.