Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution
- University of Vienna, Austria
- University of Manchester, United Kingdom
- CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Medical University of Vienna, Austria
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 were non-photosensory. A molecular profiling approach in the marine bristleworm Platynereis dumerilii revealed shared and distinct features of cephalic and non-cephalic of 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 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.
Data availability
All metadata and source files are available for download from Dryad (doi:10.5061/dryad.m63xsj416).This includes raw data, scripts, and the newly assembled and size-filtered transcriptome, used for quantitative mapping (cf. section on Transcriptome profiling).
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Metadata for the characterization of Platynereis dumerilii cephalic and non-cephalic sensory cell typeshttps://creativecommons.org/publicdomain/zero/1.0/.
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Metadata for the characterization of Platynereis dumerilii cephalic and non-cephalic sensory cell typeshttps://creativecommons.org/publicdomain/zero/1.0/.
Article and author information
Author details
Vinoth Babu Veedin Rajan
Kristin Tessmar-Raible
Funding
FP7 Ideas: European Research Council (FP7/2007-2013)/ERC Grant Agreement 260304)
- Florian Raible
Austrian Science Fund (P30035)
- Florian Raible
FP7 Ideas: European Research Council (ERC Grant Agreement 337011)
- Kristin Tessmar-Raible
H2020 European Research Council (ERC Grant Agreement 819952)
- Kristin Tessmar-Raible
Universität Wien (Research Platform Rhythms of Life"")
- Florian Raible
- Kristin Tessmar-Raible
Universität Wien (Research Platform Single-cell genomics of stem cells"")
- Florian Raible
Austrian Science Fund (START award,project Y413)
- Kristin Tessmar-Raible
Austrian Science Fund (P28970)
- Kristin Tessmar-Raible
Austrian Science Fund (I2972)
- Florian Raible
Austrian Science Fund (SFB F78)
- Florian Raible
- Kristin Tessmar-Raible
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Claude Desplan, New York University, United States
Ethics
Animal experimentation: All animal research and husbandry was conducted according to Austrian and European guidelines for animal research (fish maintenance and care approved under: BMWFW-66.006/0012-WF/II/3b/2014, experiments approved under: BMWFW-66.006/0003-WF/V/3b/2016
Version history
- Received: December 30, 2020
- Preprint posted: January 12, 2021 (view preprint)
- Accepted: August 4, 2021
- Accepted Manuscript published: August 5, 2021 (version 1)
- Version of Record published: August 16, 2021 (version 2)
Copyright
© 2021, Revilla-i-Domingo et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Characterization of cephalic and non-cephalic sensory cell types provides insight into joint photo- and mechanoreceptor evolution
eLife 10:e66144.
https://doi.org/10.7554/eLife.66144
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