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Viral rhodopsins 1 are an unique family of light-gated cation channels

Author

Listed:
  • Dmitrii Zabelskii

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich GmbH
    Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology)

  • Alexey Alekseev

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich GmbH
    Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology
    Institute of Crystallography, University of Aachen (RWTH))

  • Kirill Kovalev

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich GmbH
    Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology
    Institute of Crystallography, University of Aachen (RWTH))

  • Vladan Rankovic

    (Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen
    Auditory Neuroscience and Optogenetics Laboratory, German Primate Center)

  • Taras Balandin

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich GmbH)

  • Dmytro Soloviov

    (Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology
    Joint Institute for Nuclear Research
    Institute for Safety Problems of Nuclear Power Plants, NAS of Ukraine)

  • Dmitry Bratanov

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich GmbH)

  • Ekaterina Savelyeva

    (Institute of Biological Information Processing (IBI-3: Bioelectronics), Forschungszentrum Jülich GmbH
    Laboratory of Functional Materials and Devices for Nanoelectronics, Moscow Institute of Physics and Technology
    Center of Shared Research Facilities, Moscow Institute of Physics and Technology)

  • Elizaveta Podolyak

    (Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology)

  • Dmytro Volkov

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich GmbH)

  • Svetlana Vaganova

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich GmbH)

  • Roman Astashkin

    (Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology
    Institut de Biologie Structurale (IBS), Université Grenoble Alpes, CEA, CNRS)

  • Igor Chizhov

    (Institute for Biophysical Chemistry, Hannover Medical School)

  • Natalia Yutin

    (National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health)

  • Maksim Rulev

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich GmbH
    European Synchrotron Radiation Facility)

  • Alexander Popov

    (European Synchrotron Radiation Facility)

  • Ana-Sofia Eria-Oliveira

    (Institut de Biologie Structurale (IBS), Université Grenoble Alpes, CEA, CNRS)

  • Tatiana Rokitskaya

    (Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University)

  • Thomas Mager

    (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)

  • Yuri Antonenko

    (Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University)

  • Riccardo Rosselli

    (Evolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel Hernández
    Royal Netherland Institute for Sea Research (NIOZ), and Utrecht University)

  • Grigoriy Armeev

    (Biological Faculty, M. V. Lomonosov Moscow State University)

  • Konstantin Shaitan

    (Biological Faculty, M. V. Lomonosov Moscow State University
    N. N. Semenov Institute of Chemical Physics, Russian Academy of Sciences)

  • Michel Vivaudou

    (Institut de Biologie Structurale (IBS), Université Grenoble Alpes, CEA, CNRS
    Laboratories of Excellence, Ion Channel Science and Therapeutics)

  • Georg Büldt

    (Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology)

  • Andrey Rogachev

    (Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology
    Joint Institute for Nuclear Research)

  • Francisco Rodriguez-Valera

    (Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology
    Evolutionary Genomics Group, Departamento de Producción Vegetal y Microbiología, Universidad Miguel Hernández)

  • Mikhail Kirpichnikov

    (Biological Faculty, M. V. Lomonosov Moscow State University
    M. M. Shemyakin-Yu. A. Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences)

  • Tobias Moser

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

  • Andreas Offenhäusser

    (Institute of Biological Information Processing (IBI-3: Bioelectronics), Forschungszentrum Jülich GmbH)

  • Dieter Willbold

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich GmbH
    Institut für Physikalische Biologie, Heinrich Heine University Düsseldorf)

  • Eugene Koonin

    (National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health)

  • Ernst Bamberg

    (Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology
    Max Planck Institute of Biophysics)

  • Valentin Gordeliy

    (Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
    JuStruct: Jülich Center for Structural Biology, Forschungszentrum Jülich GmbH
    Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology
    Institute of Crystallography, University of Aachen (RWTH))

Abstract

Phytoplankton is the base of the marine food chain as well as oxygen and carbon cycles and thus plays a global role in climate and ecology. Nucleocytoplasmic Large DNA Viruses that infect phytoplankton organisms and regulate the phytoplankton dynamics encompass genes of rhodopsins of two distinct families. Here, we present a functional and structural characterization of two proteins of viral rhodopsin group 1, OLPVR1 and VirChR1. Functional analysis of VirChR1 shows that it is a highly selective, Na+/K+-conducting channel and, in contrast to known cation channelrhodopsins, it is impermeable to Ca2+ ions. We show that, upon illumination, VirChR1 is able to drive neural firing. The 1.4 Å resolution structure of OLPVR1 reveals remarkable differences from the known channelrhodopsins and a unique ion-conducting pathway. Thus, viral rhodopsins 1 represent a unique, large group of light-gated channels (viral channelrhodopsins, VirChR1s). In nature, VirChR1s likely mediate phototaxis of algae enhancing the host anabolic processes to support virus reproduction, and therefore, might play a major role in global phytoplankton dynamics. Moreover, VirChR1s have unique potential for optogenetics as they lack possibly noxious Ca2+ permeability.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-19457-7
    DOI: 10.1038/s41467-020-19457-7
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    Cited by:

    1. 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.

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