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

Dmitrii Zabelskii, Alexey Alekseev, Kirill Kovalev, Vladan Rankovic, Taras Balandin, Dmytro Soloviov, Dmitry Bratanov, Ekaterina Savelyeva, Elizaveta Podolyak, Dmytro Volkov, Svetlana Vaganova, Roman Astashkin, Igor Chizhov, Natalia Yutin, Maksim Rulev, Alexander Popov, Ana-Sofia Eria-Oliveira, Tatiana Rokitskaya, Thomas Mager, Yuri Antonenko, Riccardo Rosselli, Grigoriy Armeev, Konstantin Shaitan, Michel Vivaudou, Georg Büldt, Andrey Rogachev, Francisco Rodriguez-Valera, Mikhail Kirpichnikov, Tobias Moser, Andreas Offenhäusser, Dieter Willbold, Eugene Koonin, Ernst Bamberg and Valentin Gordeliy ()
Additional contact information
Dmitrii Zabelskii: Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
Alexey Alekseev: Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
Kirill Kovalev: Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
Vladan Rankovic: Institute for Auditory Neuroscience and InnerEarLab, University Medical Center Göttingen
Taras Balandin: Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
Dmytro Soloviov: Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology
Dmitry Bratanov: Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
Ekaterina Savelyeva: Institute of Biological Information Processing (IBI-3: Bioelectronics), Forschungszentrum Jülich GmbH
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
Svetlana Vaganova: Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH
Roman Astashkin: Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology
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
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
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
Grigoriy Armeev: Biological Faculty, M. V. Lomonosov Moscow State University
Konstantin Shaitan: Biological Faculty, M. V. Lomonosov Moscow State University
Michel Vivaudou: Institut de Biologie Structurale (IBS), Université Grenoble Alpes, CEA, CNRS
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
Francisco Rodriguez-Valera: Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow Institute of Physics and Technology
Mikhail Kirpichnikov: Biological Faculty, M. V. Lomonosov Moscow State University
Tobias Moser: Institute for Auditory Neuroscience and InnerEarLab, University Medical Center 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
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
Valentin Gordeliy: Institute of Biological Information Processing (IBI-7: Structural Biochemistry), Forschungszentrum Jülich GmbH

Nature Communications, 2020, vol. 11, issue 1, 1-16

Abstract: 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.

Date: 2020
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DOI: 10.1038/s41467-020-19457-7

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