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

• Published in: Nature communications Vol. 11; no. 1; pp. 5707 - 16
• Main Authors: Zabelskii, Dmitrii, Alekseev, Alexey, Kovalev, Kirill, Rankovic, Vladan, Balandin, Taras, Soloviov, Dmytro, Bratanov, Dmitry, Savelyeva, Ekaterina, Podolyak, Elizaveta, Volkov, Dmytro, Vaganova, Svetlana, Astashkin, Roman, Chizhov, Igor, Yutin, Natalia, Rulev, Maksim, Popov, Alexander, Eria-Oliveira, Ana-Sofia, Rokitskaya, Tatiana, Mager, Thomas, Antonenko, Yuri, Rosselli, Riccardo, Armeev, Grigoriy, Shaitan, Konstantin, Vivaudou, Michel, Büldt, Georg, Rogachev, Andrey, Rodriguez-Valera, Francisco, Kirpichnikov, Mikhail, Moser, Tobias, Offenhäusser, Andreas, Willbold, Dieter, Koonin, Eugene, Bamberg, Ernst, Gordeliy, Valentin
• Format: Journal Article
• Language: English
• Published: England Nature Publishing Group 11.11.2020; Nature Publishing Group UK; Nature Portfolio
• Subjects: Algae; Animals; Biochemistry, Molecular Biology; Calcium - metabolism; Calcium ions; Calcium permeability; Carbon cycle; Cations; Cells, Cultured; Channelrhodopsins - metabolism; Crystal structure; Deoxyribonucleic acid; DNA; DNA viruses; Food chains; Functional analysis; Genetics; HEK293 Cells; Humans; Information processing; Ion Channel Gating; Ion channels; Life Sciences; Light; Microorganisms; Neurons - metabolism; Optics; Phototaxis; Phylogeny; Phytoplankton; Phytoplankton - virology; Plankton; Protein Conformation; Proteins; Rats, Wistar; Rhodopsin; Rhodopsin - chemistry; Rhodopsin - genetics; Rhodopsin - metabolism; Structural analysis; Structural Biology; Structure-Activity Relationship; Structure-function relationships; Viral Proteins - chemistry; Viral Proteins - genetics; Viral Proteins - metabolism; Viruses; X-Ray Diffraction
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-19457-7

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 Ca 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 Ca permeability.