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

  1. Roger Revilla-i-Domingo
  2. Vinoth Babu Veedin Rajan
  3. Monika Waldherr
  4. Günther Prohaczka
  5. Hugo Musset
  6. Lukas Orel
  7. Elliot Gerrard
  8. Moritz Smolka
  9. Alexander Stockinger
  10. Matthias Farlik
  11. Robert J Lucas
  12. Florian Raible  Is a corresponding author
  13. Kristin Tessmar-Raible  Is a corresponding author
  1. University of Vienna, Austria
  2. University of Manchester, United Kingdom
  3. 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).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Roger Revilla-i-Domingo

    Max F Perutz Laboratories/ Research Platform Rhythms of Life, University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  2. Vinoth Babu Veedin Rajan

    Max F Perutz Laboratories, University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2430-7395
  3. Monika Waldherr

    Max F Perutz Laboratories/ Research Platform Rhythms of Life, University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  4. Günther Prohaczka

    Max F Perutz Laboratories/ Research Platform Rhythms of Life, University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  5. Hugo Musset

    Computational Neuroscience Unit, University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  6. Lukas Orel

    Max F Perutz Laboratories/ Research Platform Rhythms of Life, University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  7. Elliot Gerrard

    Faculty of Biology Medicine and Health, University of Manchester, Manchester, United Kingdom
    Competing interests
    No competing interests declared.
  8. Moritz Smolka

    Center for Integrative Bioinformatics Vienna, University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8621-600X
  9. Alexander Stockinger

    Center for Integrative Bioinformatics Vienna, University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
  10. Matthias Farlik

    Department of Dermatology, CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Medical University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0698-2992
  11. Robert J Lucas

    Faculty of Biology Medicine and Health, University of Manchester, Manchester, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1088-8029
  12. Florian Raible

    Max F Perutz Laboratories/ Research Platform Rhythms of Life, University of Vienna, Vienna, Austria
    For correspondence
    florian.raible@mfpl.ac.at
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4515-6485
  13. Kristin Tessmar-Raible

    Max F Perutz Laboratories/ Research Platform Rhythms of Life, University of Vienna, Vienna, Austria
    For correspondence
    kristin.tessmar@mfpl.ac.at
    Competing interests
    Kristin Tessmar-Raible, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8038-1741

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

  1. Claude Desplan, New York University, United States

Publication history

  1. Received: December 30, 2020
  2. Preprint posted: January 12, 2021 (view preprint)
  3. Accepted: August 4, 2021
  4. Accepted Manuscript published: August 5, 2021 (version 1)
  5. 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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  1. Roger Revilla-i-Domingo
  2. Vinoth Babu Veedin Rajan
  3. Monika Waldherr
  4. Günther Prohaczka
  5. Hugo Musset
  6. Lukas Orel
  7. Elliot Gerrard
  8. Moritz Smolka
  9. Alexander Stockinger
  10. Matthias Farlik
  11. Robert J Lucas
  12. Florian Raible
  13. Kristin Tessmar-Raible
(2021)
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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