The rhodopsin-retinochrome system for retinal re-isomerization predates the origin of cephalopod eyes

Background The process of photoreception in most animals depends on the light induced isomerization of the chromophore retinal, bound to rhodopsin. To re-use retinal, the all-trans-retinal form needs to be re-isomerized to 11-cis-retinal, which can be achieved in different ways. In vertebrates, this mostly includes a stepwise enzymatic process called the visual cycle. The best studied re-isomerization system in protostomes is the rhodopsin-retinochrome system of cephalopods, which consists of rhodopsin, the photoisomerase retinochrome and the protein RALBP functioning as shuttle for retinal. In this study we investigate the expression of the rhodopsin-retinochrome system and functional components of the vertebrate visual cycle in a polyplacophoran mollusk, Leptochiton asellus, and examine the phylogenetic distribution of the individual components in other protostome animals. Results Tree-based orthology assignments revealed that orthologs of the cephalopod retinochrome and RALBP are present in mollusks outside of cephalopods. By mining our dataset for vertebrate visual cycle components, we also found orthologs of the retinoid binding protein RLBP1, in polyplacophoran mollusks, cephalopods and a phoronid. In situ hybridization and antibody staining revealed that L. asellus retinochrome is co-expressed in the larval chiton photoreceptor cells (PRCs) with the visual rhodopsin, RALBP and RLBP1. In addition, multiple retinal dehydrogenases are expressed in the PRCs, which might also contribute to the rhodopsin-retinochrome system. Conclusions We conclude that the rhodopsin-retinochrome system is a common feature of mollusk PRCs and predates the origin of cephalopod eyes. Our results show that this system has to be extended by adding further components, which surprisingly, are shared with vertebrates.

Femtochemistry of Rhodopsins

The review considers the spectral kinetic data obtained by us by femtosecond absorption laser spectroscopy for the photochromic reaction of retinal isomerization in animal rhodopsin (type II), namely, bovine visual rhodopsin and microbial rhodopsins (type I), such as Exiguobacterium sibiricum rhodopsin and Halobacterium salinarum bacteriorhodopsin. It is shown that the elementary act of the photoreaction of retinal isomerization in type I and type II rhodopsins can be interpreted as a transition through a conical intersection with retention of the coherence of the vibrational wave packets generated during excitation. The coherent nature of the reaction is most pronounced in visual rhodopsin as a result of the barrier-free movement along the excited surface of potential energy, which also leads to an extremely high rate of retinal isomerization compared to microbial rhodopsins. Differences in the dynamics of photochemical reactions of type I and type II rhodopsins can be related to both differences in the initial isomeric forms of their chromophores (all-trans and 11-cis retinal, respectively), as well as with the effect of the protein environment on the chromophore. Despite the practically identical values of the quantum yields of the direct photoreaction of visual rhodopsin and bacteriorhodopsin, the reverse photoreaction of visual rhodopsin is much less effective (φ = 0.15) than in the case of bacteriorhodopsin (φ = 0.81). It can be assumed that the photobiological mechanism for converting light into an information process in the evolutionarily younger visual rhodopsins (type II rhodopsins) should be more reliable than the mechanism for converting light into a photoenergetic process in the evolutionarily more ancient microbial rhodopsins (type I rhodopsins). The low value of the quantum yield of the reverse reaction of visual rhodopsin can be considered as an increase in the reliability of the forward reaction, which triggers the process of phototransduction.