Dissecting the role of Opsins in non-cephalic receptors

Animals are known to react to light stimuli, and many of these responses are mediated by a particular group of protein, so-called Opsins, that reside in the membranes of specific light-receptive cells. Opsin molecules have been dubbed after the Greek word for sight (psis). Nonetheless, the picture begins to emerge that Opsins have significant functions that are not related to their function for eyesight, and may even be older. This project addresses these enigmatic functions of Opsins in a marine bristleworm. As the team discovered, this worm does not only have Opsin-bearing light receptors eyes in its head, but also possesses related cells in each of its segments, positioned at the lower part of each legs. Interestingly, by their position as well as their molecular signature, these cells might not only be light receptors, but may as well serve to sense touch or movement (so-called mechanic stimuli). The project will explore through a number of experiments if the identified cells indeed are able to sense mechanic stimuli, if they are light receptors, or if they combine both of these functions. These experiments will not only be relevant to understand the function of these cells in the worm: Because the cells are related to cell types in other species, and also reflect a possible ancient form of receptors that were postulated years ago, the study will allow the team to gain insight into general features of such receptor cells, and also shed light on the evolutionary origin of sensory cells.

Animals are known to react to light stimuli, and many of these responses are mediated by a particular group of protein, so-called Opsins, that reside in the membranes of specific light-receptive cells. Opsin molecules have been dubbed after the Greek word for sight (psis). Nonetheless, the picture begins to emerge that Opsins have significant functions that are not related to their function for eyesight, and may even be older. In this research project, these enigmatic functions of Opsins have been studied in a marine bristleworm. As the team discovered, this worm does not only have Opsin-bearing light receptors eyes in its head, but also possesses related cells in each of its segments. Their position, as well as their expression of some marker genes, had suggested that these cells might not be regular light receptors, but possibly be related to mechanoreceptors, i.e. receptors able to sense mechanical stress or changes in pressure. The project explored this possibility in a variety of experiments. Taking advantage of an engineered strain of worms that produce a fluorescent marker in both peripheral receptors and eye photoreceptor, the team could use fluorescence-activated cell sorting (FACS) to enrich cells of both classes and characterize their molecular signature. Indeed, the peripheral cells expressed genes known to play roles in mechanoreceptors, but they also contained a specific opsin and a complete set of genes that is known to be relevant for light reception. The team further established a worm strain in which the opsin gene was disrupted, thereby interfering with light sensation. Peripheral cells isolated from such worms exhibited significant changes in their light-dependent signature. With the help of additional behavioral analyses, the team could finally show that the peripheral cells appear to have a mechanosensory function that is modulated by light via the Opsin light receptor. These results have added a novel concept to our understanding of sensory cell type evolution, providing a plausible model of why and how light receptive Opsins might be linked to mechanosensory function. This notion has relevance for both neurobiology and comparative / evolutionary developmental biology. Moreover, the establishment of the opsin knock-out worms as well as the characterization of the sensitivity of this Opsin have contributed to the discovery that the same factor is also relevant for sensing moonlight to adjust the worms' inner timing system. Together, the work has advanced insight into how environmental light impacts on sensory biology and physiology of marine animals.