Abstract

BackgroundIn metazoans, opsins are photosensitive proteins involved in both vision and non-visual photoreception. Echinoderms have no well-defined eyes but several opsin genes were found in the purple sea urchin (Strongylocentrotus purpuratus) genome. Molecular data are lacking for other echinoderm classes although many species are known to be light sensitive.ResultsIn this study focused on the European brittle star Amphiura filiformis, we first highlighted a blue-green light sensitivity using a behavioural approach. We then identified 13 new putative opsin genes against eight bona fide opsin genes in the genome of S. purpuratus. Six opsins were included in the rhabdomeric opsin group (r-opsins). In addition, one putative ciliary opsin (c-opsin), showing high similarity with the c-opsin of S. purpuratus (Sp-opsin 1), one Go opsin similar to Sp-opsins 3.1 and 3.2, two basal-branch opsins similar to Sp-opsins 2 and 5, and two neuropsins similar to Sp-opsin 8, were identified. Finally, two sequences from one putative RGR opsin similar to Sp-opsin 7 were also detected. Adult arm transcriptome analysis pinpointed opsin mRNAs corresponding to one r-opsin, one neuropsin and the homologue of Sp-opsin 2. Opsin phylogeny was determined by maximum likelihood and Bayesian analyses. Using antibodies designed against c- and r-opsins from S. purpuratus, we detected putative photoreceptor cells mainly in spines and tube feet of A. filiformis, respectively. The r-opsin expression pattern is similar to the one reported in S. purpuratus with cells labelled at the tip and at the base of the tube feet. In addition, r-opsin positive cells were also identified in the radial nerve of the arm. C-opsins positive cells, expressed in pedicellariae, spines, tube feet and epidermis in S. purpuratus were observed at the level of the spine stroma in the brittle star.ConclusionLight perception in A. filiformis seems to be mediated by opsins (c- and r-) in, at least, spines, tube feet and in the radial nerve cord. Other non-visual opsin types could participate to the light perception process indicating a complex expression pattern of opsins in this infaunal brittle star.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-1035) contains supplementary material, which is available to authorized users.

Highlights

  • In metazoans, opsins are photosensitive proteins involved in both vision and non-visual photoreception

  • The unexpected high opsin diversity and the complex opsin expression pattern in a burrowing species are reported. What these results suggest about extraocular light perception functions and opsin-based photoreception evolution in brittle stars and echinoderms is discussed

  • Spectral photosensitivity estimation in A. filiformis Behavioural experiments were performed on adult brittle stars to confirm (i) their light sensitivity and (ii) highlight their general spectral sensitivity

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Summary

Introduction

Opsins are photosensitive proteins involved in both vision and non-visual photoreception. Echinoderms have no well-defined eyes but several opsin genes were found in the purple sea urchin (Strongylocentrotus purpuratus) genome. Luminous information is mainly detected through photosensitive proteins, the opsins, which are involved in both vision and non-visual photoreception [2]. The new genetic information which was made available by the publication of the complete genome of the purple sea urchin Strongylocentrotus purpuratus [3] generated portions of epidermis [4,5,9,10]. Photoreceptors are not as uniformly scattered as researchers postulated at first but are clustered in specific organs, which together, would constitute a complex “photosensory machinery” [4,5,9,10]. The diversity of opsins seems to be related to different photoreceptor cell types and to a large variety of light-driven behaviours [9,13,14,15]

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