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bioRxiv · 10.1101/2021.01.10.426124

Analyses of cephalic and non-cephalic sensory cell types provide insight into joint photo- and mechanoreceptor evolution

Revilla-i-Domingo, R.·Rajan, V. B. V.·Waldherr, M.·Prohaczka, G.·Musset, H.·Orel, L.·Gerrard, E.·Smolka, M.·Farlik, M.·Lucas, R. J.·Raible, F.·Tessmar-Raible, K.
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Abstract

Rhabdomeric Opsins (r-Opsins) are light-sensors in cephalic eye photoreceptors, but also function in additional sensory organs. This has prompted questions on the evolutionary relationship of these cell types, and if ancient r-Opsins cells were non-photosensory. Our profiling of cephalic and non-cephalic r-opsin1-expressing cells of the marine bristleworm Platynereis dumerilii reveals shared and distinct features. Non-cephalic cells possess a full set of phototransduction components, but also a mechanosensory signature. We determine that Pdu-r-Opsin1 is a Gq-coupled blue-light receptor. Profiling of cells from r-opsin1 mutants versus wild-types, and a comparison under different light conditions reveals that in the non-cephalic cells, light - mediated by r-Opsin1 - adjusts the expression level of a calcium transporter relevant for auditory mechanosensation in vertebrates. We establish a deep learning-based quantitative behavioral analysis for animal trunk movements, and identify a light-and r-Opsin-1-dependent fine-tuning of the worms undulatory movements in headless trunks, which are known to require mechanosensory feedback. Our results suggest an evolutionary concept in which r-Opsins act as ancient, light-dependent modulators of mechanosensation, and suggest that light-independent mechanosensory roles of r-Opsins likely evolved secondarily.

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Revilla-i-Domingo, R., Rajan, V. B. V., Waldherr, M., Prohaczka, G., Musset, H., Orel, L., Gerrard, E., Smolka, M., Farlik, M., Lucas, R. J., Raible, F., Tessmar-Raible, K.. 2021-01-12. Analyses of cephalic and non-cephalic sensory cell types provide insight into joint photo- and mechanoreceptor evolution. https://doi.org/10.1101/2021.01.10.426124

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