Mechanisms of inward transmembrane proton translocation

Kirill Kovalev (1) , Fedor Tsybrov (2) , Alexey Alekseev (3, 4, 5) , Vitaly Shevchenko (3, 5, 4) , Dmytro Soloviov (2) , Sergey Siletsky (6) , Gleb Bourenkov (1) , Michael Agthe (1) , Marina Nikolova (1) , David von Stetten (7) , Roman Astashkin (8) , Sergey Bukhdruker (7, 4, 9) , Igor Chizhov (10) , Antoine Royant (8) , Alexander Kuzmin (2) , Ivan Gushchin (11) , Riccardo Rosselli (12) , Francisco Rodriguez-Valera (13) , Nikolay Ilyinskiy (2) , Andrey Rogachev (2) , Valentin Borshchevskiy (2) , Thomas Schneider (1) , Ernst Bamberg (14) , Valentin Gordeliy (8)

1 EMBL - European Molecular Biology Laboratory [Hamburg]
2 Research Center for Molecular Mechanisms of Aging and Age-related Diseases, Moscow
3 ICS - Institute of Complex Systems
4 MIPT - Moscow Institute of Physics and Technology [Moscow]
5 Institute of Crystallography [Aachen]
6 Electron Microscopy Department, AN Belozersky Institute of Physical and Chemical Biology
7 ESRF - European Synchrotron Radiation Facility [Grenoble]
8 IBS - UMR 5075 - Institut de biologie structurale
9 IBI-7 - Institute of Biological Information Processing [Jülich]
10 MHH - Medizinische Hochschule Hannover = Hannover Medical School
11 JuStruct - Jülich Center for Structural Biology [Jülich]
12 Departamento de Producción Vegetal y Microbiología
13 UMH - Universidad Miguel Hernández [Elche]
14 MPIBP - Max-Planck-Institut für Biophysik - Max Planck Institute of Biophysics

Proton transport is indispensable for cell life. It is believed that molecular mechanisms of proton movement through different types of proton-conducting molecules have general universal features. However, elucidation of such mechanisms is a challenge. It requires true-atomic-resolution structures of all key proton-conducting states. Here we present a comprehensive function-structure study of a light-driven bacterial inward proton pump, xenorhodopsin, from Bacillus coahuilensis in all major proton-conducting states. The structures reveal that proton translocation is based on proton wires regulated by internal gates. The wires serve as both selectivity filters and translocation pathways for protons. The cumulative results suggest a general concept of proton translocation. We demonstrate the use of serial time-resolved crystallography at a synchrotron source with sub-millisecond resolution for rhodopsin studies, opening the door for principally new applications. The results might also be of interest for optogenetics since xenorhodopsins are the only alternative tools to fire neurons.

Domaines: Sciences du Vivant [q-bio]

Kirill Kovalev, Fedor Tsybrov, Alexey Alekseev, Vitaly Shevchenko, Dmytro Soloviov, et al.. Mechanisms of inward transmembrane proton translocation. Nature Structural and Molecular Biology, 2023, 30 (7), pp.970-979. ⟨10.1038/s41594-023-01020-9⟩. ⟨hal-04216521⟩