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The ability to respond to light has profoundly shaped life. Animals with eyes overwhelmingly rely on their visual circuits for mediating light-induced coordinated movements. Building on previously reported behaviors, we report the discovery of an organized, eye-independent (extraocular), body-wide photosensory framework that allows even a head-removed animal to move like an intact animal. Despite possessing sensitive cerebral eyes and a centralized brain that controls most behaviors, head-removed planarians show acute, coordinated ultraviolet-A (UV-A) aversive phototaxis. We find this eye–brain-independent phototaxis is mediated by two noncanonical rhabdomeric opsins, the first known function for this newly classified opsin-clade. We uncover a unique array of dual-opsin–expressing photoreceptor cells that line the periphery of animal body, are proximal to a body-wide nerve net, and mediate UV-A phototaxis by engaging multiple modes of locomotion. Unlike embryonically developing cerebral eyes that are functional when animals hatch, the body-wide photosensory array matures postembryonically in “adult-like animals.” Notably, apart from head-removed phototaxis, the body-wide, extraocular sensory organization also impacts physiology of intact animals. Low-dose UV-A, but not visible light (ocular-stimulus), is able to arouse intact worms that have naturally cycled to an inactive/rest-like state. This wavelength selective, low-light arousal of resting animals is noncanonical-opsin dependent but eye independent. Our discovery of an autonomous, multifunctional, late-maturing, organized body-wide photosensory system establishes a paradigm in sensory biology and evolution of light sensing.

Photoreception and vision are fundamental aspects of animal sensory biology and ecology, but important gaps remain in our understanding of these processes in many species. The colour-changing brittle star Ophiocoma wendtii is iconic in vision research, speculatively possessing a unique whole-body visual system that incorporates information from nerve bundles underlying thousands of crystalline ‘microlenses’. The hypothesis that these might form a sophisticated compound eye-like system regulated by chromatophores has been extensively reiterated, with investigations into biomimetic optics and similar supposedly ‘visual’ structures in living and fossil taxa. However, no photoreceptors or visual behaviours have ever been identified. We present the first evidence of photoreceptor networks in three Ophiocoma species, both with and without microlenses and colour-changing behaviour. High-resolution microscopy, immunohistochemistry and synchrotron tomography demonstrate that putative photoreceptors cover the animals' oral, lateral and aboral surfaces, but are absent at the hypothesized focal points of the microlenses. The structural optics of these crystal ‘lenses’ are an exaptation and do not fulfil any apparent visual role. This contradicts previous studies, yet the photoreceptor network in Ophiocoma appears even more widespread than previously anticipated, both taxonomically and anatomically.

Most animals possess multiple opsins which sense light for visual and non-visual functions. Here, we show spectral characteristics of non-visual opsins, vertebrate Opn3s, which are widely distributed among vertebrates. We successfully expressed zebrafish Opn3 in mammalian cultured cells and measured its absorption spectrum spectroscopically. When incubated with 11-cis retinal, zebrafish Opn3 formed a blue-sensitive photopigment with an absorption maximum around 465 nm. The Opn3 converts to an all-trans retinal-bearing photoproduct with an absorption spectrum similar to the dark state following brief blue-light irradiation. The photoproduct experienced a remarkable blue-shift, with changes in position of the isosbestic point, during further irradiation. We then used a cAMP-dependent luciferase reporter assay to investigate light-dependent cAMP responses in cultured cells expressing zebrafish, pufferfish, anole and chicken Opn3. The wild type opsins did not produce responses, but cells expressing chimera mutants (WT Opn3s in which the third intracellular loops were replaced with the third intracellular loop of a Gs-coupled jellyfish opsin) displayed light-dependent changes in cAMP. The results suggest that Opn3 is capable of activating G protein(s) in a light-dependent manner. Finally, we used this assay to measure the relative wavelength-dependent response of cells expressing Opn3 chimeras to multiple quantally-matched stimuli. The inferred spectral sensitivity curve of zebrafish Opn3 accurately matched the measured absorption spectrum. We were unable to estimate the spectral sensitivity curve of mouse or anole Opn3, but, like zebrafish Opn3, the chicken and pufferfish Opn3-JiL3 chimeras also formed blue-sensitive pigments. These findings suggest that vertebrate Opn3s may form blue-sensitive G protein-coupled pigments. Further, we suggest that the method described here, combining a cAMP-dependent luciferase reporter assay with chimeric opsins possessing the third intracellular loop of jellyfish opsin, is a versatile approach for estimating absorption spectra of opsins with unknown signaling cascades or for which absorption spectra are difficult to obtain.

Molecular research on the evolution of extraocular photoreception has drawn attention to photosensitive animals lacking proper eye organs. Outside of vertebrates, little is known about this type of sensory system in any other deuterostome. In this study, we investigate such an extraocular photoreceptor cell (PRC) system in developmental stages of the sea urchin Paracentrotus lividus. We provide a general overview of the cell type families present at the mature rudiment stage using single-cell transcriptomics, while emphasizing the PRCs complexity. We show that three neuronal and one muscle-like PRC type families express retinal genes prior to metamorphosis. Two of the three neuronal PRC type families express a rhabdomeric opsin as well as an echinoderm-specific opsin (echinopsin), and their genetic wiring includes sea urchin orthologs of key retinal genes such as hlf, pp2ab56e, barh, otx, ac/sc, brn3, six1/2, pax6, six3, neuroD, irxA, isl and ato. Using qPCR, in situ hybridization, and immunohistochemical analysis, we found that the expressed retinal gene composition becomes more complex from mature rudiment to juvenile stage. The majority of retinal genes are expressed dominantly in the animals’ podia, and in addition to the genes already expressed in the mature rudiment, the juvenile podia express a ciliary opsin, another echinopsin, and two Go-opsins. The expression of a core of vertebrate retinal gene orthologs indicates that sea urchins have an evolutionarily conserved gene regulatory toolkit that controls photoreceptor specification and function, and that their podia are photosensory organs.

To sense light, animals often utilize mechanisms that rely on visual pigments composed of opsin and retinal. The photon-induced isomerization of 11- cis -retinal to the all- trans configuration triggers phototransduction cascades, resulting in a change in the membrane potential of the photoreceptor. In mollusks, the most abundant opsin in the eye is Gq-coupled rhodopsin (Gq-rhodopsin). The Gq-rhodopsin-based visual pigment is bistable, with the regeneration of 11- cis -retinal occurring in a light-dependent manner without leaving the opsin moiety. 11- cis -retinal is also regenerated by the action of retinochrome in the cell bodies. Retinal binding protein (RALBP) mediates retinal transport between Gq-rhodopsin and retinochrome in the cytoplasm. However, recent studies have identified additional bistable opsins in mollusks, including Opn5 and xenopsin. It is unknown whether these bistable opsins require RALBP and retinochrome for the continuous regeneration of 11- cis -retinal. In the present study, we examined the expression of RALBP and retinochrome in the photoreceptors expressing Opn5 or Xenopsin in the heterobranch gastropods Limax and Peronia . Our findings revealed that retinochrome, but not RALBP, was present in some of the Opn5A-positive brain photosensory neurons of Limax . The ciliary cells in the dorsal eye of Peronia , which express Xenopsin2, lacked both retinochrome and RALBP. Therefore, bistable opsins do not necessarily depend on the RALBP-retinochrome system in a cell. We also examined the expression of other proteins that support visual function, such as β-arrestin, Gq, and Go, in all types of photoreceptors in these animals, and uncovered differences in the molecular composition among the photoreceptors.

Bioluminescence is a common phenomenon in marine organisms, especially in deep water where faint blue light remains. Among elasmobranchs, three families display the ability to emit light, the Etmopteridae, the Dalatiidae, and the Somniosidae. Luminous sharks have thousands of minute light organs, called photophores, that are mainly present ventrally and produce light. The main function of shark luminescence is counterillumination to camouflage the shark silhouette by mimicking the residual ambient light and avoiding being spotted by predators underneath. To perform counterillumination efficiently, luminescence needs to be finely adjusted. A new type of control was recently demonstrated via extraocular photoreception at the level of the light organ. An encephalopsin (i.e., opsin 3) was shown to be expressed in the vicinity of the photophore of an Etmopteridae species, Etmopterus spinax. This opsin was also demonstrated to be expressed concomitantly with the photophore development (i.e., when photophores become able to produce light) during E. spinax embryogenesis. To understand the photophore morphogenesis of different shark families, we analyzed the smalleye pygmy shark, Squaliolus aliae, with a photophore formation which represents the first report on the Dalatiidae family. Since Dalatiidae and Etmopteridae are phylogenetically closely related, the photophore morphogenesis was compared with an Etmopteridae representative, Etmopterus spinax. The results also reveal that Squaliolus aliae shares similar encephalopsin expression pattern as in Etmopterus spinax, which further supports evolutionary conservation of photophore morphogenesis as well as its own encephalopsin-based light perception across the two luminous shark families.

While the concept of a dermal light sense has existed for over a century, little progress has been made in our understanding of the mechanisms underlying dispersed photoreception and the evolutionary histories of dispersed photoreceptor cells. These cells historically have been difficult to locate and positively identify, but modern molecular techniques, integrated with existing behavioral, morphological, and physiological data, will make cell identification easier and allow us to address questions of mechanism and evolution. With this in mind, we propose a new classification scheme for all photoreceptor cell types based on two axes, cell distribution (aggregated vs. dispersed) and position within neural networks (first order vs. high order). All photoreceptor cells fall within one of four quadrants created by these axes: aggregated/high order, dispersed/high order, aggregated/first order, or dispersed/first order. This new method of organization will help researchers make objective comparisons between different photoreceptor cell types. Using integrative data from four major phyla (Mollusca, Cnidaria, Echinodermata, and Arthropoda), we also provide evidence for three hypotheses for dispersed photoreceptor cell function and evolution. First, aside from echinoderms, we find that animals often use dispersed photoreceptor cells for tasks that do not require spatial vision. Second, although there are both echinoderm and arthropod exceptions, we find that dispersed photoreceptor cells generally lack morphological specializations that either enhance light gathering or aid in the collection of directional information about light. Third, we find that dispersed photoreceptor cells have evolved a number of times in Metazoa and that most dispersed photoreceptor cells have likely evolved through the co-option of existing phototransduction cascades. Our new classification scheme, combined with modern investigative techniques, will help us address these hypotheses in great detail and generate new hypothesis regarding the function and evolution of dispersed photoreceptor cells.