R. Astashkin, G. A. Armeev, Natalia Yutin, Andreas Offenhäusser, Ekaterina Savelyeva, Kirill Kovalev, Igor Chizhov, Dmitrii Zabelskii, Francisco Rodriguez-Valera, Ernst Bamberg, Alexander Popov, Vladan Rankovic, Maksim Rulev, Dmitry Bratanov, Valentin Gordeliy, Alexey Alekseev, Michel Vivaudou, D V Soloviov, Riccardo Rosselli, Taras Balandin, Tatiana I. Rokitskaya, Eugene V. Koonin, Georg Büldt, Svetlana Vaganova, Ana-Sofia Eria-Oliveira, Yuri N. Antonenko, Tobias Moser, Mikhail P. Kirpichnikov, A. V. Rogachev, Thomas Mager, Dieter Willbold, Elizaveta Podolyak, Dmytro Volkov, Konstantin V. Shaitan, Institute of Biological Information Processing [Jülich] (IBI-7), Institut de biologie structurale (IBS - UMR 5075), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Grenoble Alpes (UGA), Institute for Auditory Neuroscience and InnerEarLab, Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow, Hannover Medical School [Hannover] (MHH), National Center for Biotechnology Information (NCBI), European Synchrotron Radiation Facility (ESRF), Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University (MSU), Max-Planck-Institut für Biophysik - Max Planck Institute of Biophysics (MPIBP), Max-Planck-Gesellschaft, Departamento de Producción Vegetal y Microbiología, Universidad Miguel Hernández [Elche] (UMH), Lomonosov Moscow State University, Biological Faculty, N. N. Semenov Institute of Chemical Physics, Russian Academy of Sciences [Moscow] (RAS), InnerEarLab, Department of Otolaryngology and Center for Molecular Physiology of the Brain-Georg-August-University = Georg-August-Universität Göttingen, National Center for Biotechnology Information, National Institutes of Health, Department of Health and Human Services, Bethesda, Md, National Institutes of Health [Bethesda] (NIH), ANR-17-EURE-0003,CBH-EUR-GS,CBH-EUR-GS(2017), ANR-19-CE11-0026,Viral_Rhodopsins,Rhodopsines virales: Structure, Fonction, et Nouveaux Outils pour l'Optogénétique(2019), and Department of Otolaryngology and Center for Molecular Physiology of the Brain-University of Göttingen - Georg-August-Universität Göttingen
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., Nucleocytoplasmic Large DNA Viruses (NCLDV) that infect algae encode two distinct families of microbial rhodopsins. Here, the authors characterise two proteins form the viral rhodopsin group 1 OLPVR1 and VirChR1, present the 1.4 Å crystal structure of OLPVR1 and show that viral rhodopsins 1 are light-gated cation channels.