Feeding and growth are regulated by light and opsins-mediated phototransduction in sea cucumber Apostichopus japonicus

Light is a crucial environmental ecological factor that affects physiological processes including feeding and growth of marine invertebrates. Although nonvisual photosensitivity has long been known in echinoderms, the underlying molecular regulation mechanism remains unclear. Here, we firstly reported opsins-mediated phototransduction signaling and the cross-talk between light and feeding/growth in Apostichopus japonicus, an important economic species with high medicinal and nutritional values. Molecular characterization analysis of Ajopsins revealed that they were mainly distributed in the epidermis of potential photosensitive tissues (tentacles, papillae and tube feet). And all four Ajopsins including Rhodopsin 5-like (AjRH5), long-wavelength-sensitive opsin (AjLWS), peropsin (AjPOP), and peropsin-like (AjPOPL) exhibited different expression patterns in response to different light conditions. Moreover, four Ajopsins all conjugated with Gαi/o to reduce intracellular cAMP levels. Besides, three Ajopsins (AjRH5, AjPOP and AjPOPL) conjugated with Gαq to activate Gαq/Ca2+/PKC signaling. And all four opsins could activate downstream ERK1/2 phosphorylation. In addition, the photosensitivities of these four Ajopsins were different in response to different wavelength of light, AjPOP and AjPOPL were sensitive to short-medium-long wavelength light, AjRH5 and AjLWS were sensitive to medium-long wavelength light. Furthermore, indoor aquaculture experiment showed that 150 lx and 300 lx light intensity could significantly promote feeding and growth of A. japonicus, which might be mediated by AjOXP1 and AjMAP2K4. Under different light wavelength treatment, red light (655–665 nm) significantly promoted the feeding and growth of A. japonicus, which may be mediated by AjOXP1/2, AjMAP2K4 and AjMegf6. And siRNA experiment further confirmed the crosstalk between AjPOPL and AjOXP1, suggesting AjPOPL may regulate feeding by AjOXP1 in A. japonicus. Our findings showed a comprehensive description of Ajopsins signaling, providing new insights on the molecular mechanism of photoreception involved in regulating feeding and growth in A. japonicus and suggested the optimum light conditions for optimizing the lighting scheme of A. japonicus aquaculture.