TY - JOUR TI - Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution AU - Revilla-i-Domingo, Roger AU - Rajan, Vinoth Babu Veedin AU - Waldherr, Monika AU - Prohaczka, Günther AU - Musset, Hugo AU - Orel, Lukas AU - Gerrard, Elliot AU - Smolka, Moritz AU - Stockinger, Alexander AU - Farlik, Matthias AU - Lucas, Robert J AU - Raible, Florian AU - Tessmar-Raible, Kristin A2 - Desplan, Claude A2 - Bronner, Marianne E A2 - Oakley, Todd A2 - Schlosser, Gerhard VL - 10 PY - 2021 DA - 2021/08/05 SP - e66144 C1 - eLife 2021;10:e66144 DO - 10.7554/eLife.66144 UR - https://doi.org/10.7554/eLife.66144 AB - 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 were non-photosensory. A molecular profiling approach in the marine bristleworm Platynereis dumerilii revealed shared and distinct features of cephalic and non-cephalic r-opsin1-expressing cells. Non-cephalic cells possess a full set of phototransduction components, but also a mechanosensory signature. Prompted by the latter, we investigated Platynereis putative mechanotransducer and found that nompc and pkd2.1 co-expressed with r-opsin1 in TRE cells by HCR RNA-FISH. To further assess the role of r-Opsin1 in these cells, we studied its signaling properties and unraveled that r-Opsin1 is a Gαq-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 worm's undulatory movements in headless trunks, which are known to require mechanosensory feedback. Our results provide new data on peripheral cell types of likely light sensory/mechanosensory nature. These results point towards a concept in which such a multisensory cell type evolved to allow for fine-tuning of mechanosensation by light. This implies that light-independent mechanosensory roles of r-opsins may have evolved secondarily. KW - photoreceptor KW - opsin KW - evolution KW - behavior JF - eLife SN - 2050-084X PB - eLife Sciences Publications, Ltd ER -