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Hijacking of internal calcium dynamics by intracellularly residing viral rhodopsins

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  • Ana-Sofia Eria-Oliveira

    (Univ. Grenoble Alpes, CEA, CNRS, IBS
    Université Côte d’Azur, CNRS, INSERM, iBV
    Ion Channel Science and Therapeutics
    Fédération Hospitalo-Universitaire InovPain, Cote d’Azur University, University Hospital Center Nice)

  • Mathilde Folacci

    (Univ. Grenoble Alpes, CEA, CNRS, IBS
    Ion Channel Science and Therapeutics
    Aarhus University)

  • Anne Amandine Chassot

    (Université Côte d’Azur, CNRS, INSERM, iBV
    Ion Channel Science and Therapeutics
    Fédération Hospitalo-Universitaire InovPain, Cote d’Azur University, University Hospital Center Nice)

  • Sandrine Fedou

    (Univ. Bordeaux, Inserm, BRIC, UMR)

  • Nadine Thézé

    (Univ. Bordeaux, Inserm, BRIC, UMR)

  • Dmitrii Zabelskii

    (European XFEL)

  • Alexey Alekseev

    (Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen
    Cluster of Excellence “Multiscale Bioimaging: from Molecular Machines to Networks of Excitable Cells” (MBExC), University of Göttingen)

  • Ernst Bamberg

    (Max Planck Institute of Biophysics)

  • Valentin Gordeliy

    (Univ. Grenoble Alpes, CEA, CNRS, IBS
    Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich)

  • Guillaume Sandoz

    (Université Côte d’Azur, CNRS, INSERM, iBV
    Ion Channel Science and Therapeutics
    Fédération Hospitalo-Universitaire InovPain, Cote d’Azur University, University Hospital Center Nice)

  • Michel Vivaudou

    (Univ. Grenoble Alpes, CEA, CNRS, IBS
    Ion Channel Science and Therapeutics)

Abstract

Rhodopsins are ubiquitous light-driven membrane proteins with diverse functions, including ion transport. Widely distributed, they are also coded in the genomes of giant viruses infecting phytoplankton where their function is not settled. Here, we examine the properties of OLPVR1 (Organic Lake Phycodnavirus Rhodopsin) and two other type 1 viral channelrhodopsins (VCR1s), and demonstrate that VCR1s accumulate exclusively intracellularly, and, upon illumination, induce calcium release from intracellular IP3-dependent stores. In vivo, this light-induced calcium release is sufficient to remote control muscle contraction in VCR1-expressing tadpoles. VCR1s natively confer light-induced Ca2+ release, suggesting a distinct mechanism for reshaping the response to light of virus-infected algae. The ability of VCR1s to photorelease calcium without altering plasma membrane electrical properties marks them as potential precursors for optogenetics tools, with potential applications in basic research and medicine.

Suggested Citation

  • Ana-Sofia Eria-Oliveira & Mathilde Folacci & Anne Amandine Chassot & Sandrine Fedou & Nadine Thézé & Dmitrii Zabelskii & Alexey Alekseev & Ernst Bamberg & Valentin Gordeliy & Guillaume Sandoz & Michel, 2024. "Hijacking of internal calcium dynamics by intracellularly residing viral rhodopsins," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44548-6
    DOI: 10.1038/s41467-023-44548-6
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    References listed on IDEAS

    as
    1. Dmitry Bratanov & Kirill Kovalev & Jan-Philipp Machtens & Roman Astashkin & Igor Chizhov & Dmytro Soloviov & Dmytro Volkov & Vitaly Polovinkin & Dmitrii Zabelskii & Thomas Mager & Ivan Gushchin & Taty, 2019. "Unique structure and function of viral rhodopsins," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Mohammad Moniruzzaman & Carolina A. Martinez-Gutierrez & Alaina R. Weinheimer & Frank O. Aylward, 2020. "Dynamic genome evolution and complex virocell metabolism of globally-distributed giant viruses," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    3. Dmitrii Zabelskii & Alexey Alekseev & Kirill Kovalev & Vladan Rankovic & Taras Balandin & Dmytro Soloviov & Dmitry Bratanov & Ekaterina Savelyeva & Elizaveta Podolyak & Dmytro Volkov & Svetlana Vagano, 2020. "Viral rhodopsins 1 are an unique family of light-gated cation channels," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
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