Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution

eLife

Matthias Farlik¹  Elliot Gerrard²  Robert J Lucas²  Vinoth Babu Veedin Rajan³  Günther Prohaczka³  Monika Waldherr³  Kristin Tessmar-Raible³  Hugo Musset³  Lukas Orel³  Moritz Smolka⁴  Florian Raible⁵  Roger Revilla-i-Domingo⁵  Alexander Stockinger⁵ 

[1] CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Vienna, Austria;Department of Dermatology, Medical University of Vienna, Vienna, Austria;Division of Neuroscience & Experimental Psychology, University of Manchester, Manchester, United Kingdom;Max Perutz Labs, University of Vienna, Vienna BioCenter, Vienna, Austria;Research Platform “Rhythms of Life”, University of Vienna, Vienna BioCenter, Vienna, Austria;Max Perutz Labs, University of Vienna, Vienna BioCenter, Vienna, Austria;Research Platform “Rhythms of Life”, University of Vienna, Vienna BioCenter, Vienna, Austria;Center for Integrative Bioinformatics Vienna, Max Perutz Labs, University of Vienna and Medical University of Vienna, Vienna, Austria;Max Perutz Labs, University of Vienna, Vienna BioCenter, Vienna, Austria;Research Platform “Rhythms of Life”, University of Vienna, Vienna BioCenter, Vienna, Austria;Research Platform "Single-Cell Regulation of Stem Cells", University of Vienna, Vienna BioCenter, Vienna, Austria;

关键词: photoreceptor;    opsin;    evolution;    behavior;    P. dumerilii;   

DOI  :  10.7554/eLife.66144

来源: eLife Sciences Publications, Ltd

【 摘 要 】

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.

【 授权许可】

CC BY