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.
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
Reviewing Editor
- Claude Desplan, New York University, United States
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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Cephalochordates and tunicates represent the only two groups of invertebrate chordates, and extant cephalochordates – commonly known as amphioxus or lancelets – are considered the best proxy for the chordate ancestor, from which they split around 520 million years ago. Amphioxus has been an important organism in the fields of zoology and embryology since the 18th century, and the morphological and genomic simplicity of cephalochordates (compared to vertebrates) makes amphioxus an attractive model for studying chordate biology at the cellular and molecular levels. Here we describe the life cycle of amphioxus, and discuss the natural histories and habitats of the different species of amphioxus. We also describe their use as laboratory animal models, and discuss the techniques that have been developed to study different aspects of amphioxus.
