A ciliary opsin in the brain of a marine annelid zooplankton is ultraviolet-sensitive, and the sensitivity is tuned by a single amino acid residue

Abstract

Ciliary opsins were classically thought to function only in vertebrates for vision, but they have also been identified recently in invertebrates for non-visual photoreception. Larvae of the annelid are used as a zooplankton model, and this zooplankton species possesses a "vertebrate-type" ciliary opsin (named c-opsin) in the brain. c-opsin is suggested to relay light signals for melatonin production and circadian behaviors. Thus, the spectral and biochemical characteristics of this c-opsin would be directly related to non-visual photoreception in this zooplankton model. Here we demonstrate that the c-opsin can sense UV to activate intracellular signaling cascades and that it can directly bind exogenous all--retinal. These results suggest that this c-opsin regulates circadian signaling in a UV-dependent manner and that it does not require a supply of 11--retinal for photoreception. Avoidance of damaging UV irradiation is a major cause of large-scale daily zooplankton movement, and the observed capability of the c-opsin to transmit UV signals and bind all-retinal is ideally suited for sensing UV radiation in the brain, which presumably lacks enzymes producing 11--retinal. Mutagenesis analyses indicated that a unique amino acid residue (Lys-94) is responsible for c-opsin-mediated UV sensing in the brain. We therefore propose that acquisition of the lysine residue in the c-opsin would be a critical event in the evolution of to enable detection of ambient UV light. In summary, our findings indicate that the c-opsin possesses spectral and biochemical properties suitable for UV sensing by the zooplankton model.

Ciliary and rhabdomeric photoreceptor-cell circuits form a spectral depth gauge in marine zooplankton

“…Next, we expressed Platynereis c-opsin1 in COS1 cells, reconstituted it with 11-cis-retinal and purified it (Yokoyama, 2000). The reconstituted pigment absorbed in the UV range with a λ-max of 384 nm in the dark spectrum and a λ-max of 370 nm in the dark-light difference spectrum ( Figure 2E), in agreement with a recent report (Tsukamoto et al, 2017). To investigate how cPRCs respond to light, we did calcium imaging in larvae ubiquitously expressing the calcium sensor GCaMP6s (Chen et al, 2013;.…”

“…The pigmented eyes mediate early-and late-stage larval phototaxis (Gühmann et al, 2015;Jékely et al, 2008;Randel et al, 2014). The cPRCs in Platynereis have been proposed to regulate melatonin production and to entrain the circadian clock to ambient UV light (Arendt et al, 2004;Tosches et al, 2014;Tsukamoto et al, 2017). However, the function of the cPRCs in Platynereis and how they interact with rPRCs is still unknown.…”

Electrophysiology and transcriptomics reveal two photoreceptor classes and complex visual integration inHirudo verbana

“…Of the two putative opsins found in Hirudo, one (Contig139791, Supplemental File) had BLAST hits with other invertebrate opsins outside of leeches that are sensitive to blue and green wavelengths; the other (Contig156444, Supplemental File) showed similarities to UV opsins from arthropods. We also performed a direct BLAST comparison against a previously described UV-sensitive from another annelid, Platynereis dumerilii (Tsukamoto et al, 2017), and found a close match between it and our putative UV opsin (Table S1).…”

A Go-type opsin mediates the shadow reflex in the annelid Platynereis dumerilii

“…4a). Pdu -c-opsin1, is maximally photo-activated between 380 and 400 nm [25], and thus can be discounted from shadow detection due to a negligible wildtype shadow response at 400 nm light (Fig. 1b).…”

“…The in vitro opsin absorption assay was conducted as described by Tsukamoto et al [25]. Briefly, native Platynereis c-opsin2 with the 1D4 tag (ETSQVAPA) on the C-termini was subcloned into the pMT vector.…”