True-atomic-resolution insights into the structure and functional role of linear chains and low-barrier hydrogen bonds in proteins

• Published in: Nature structural & molecular biology Vol. 29; no. 5; pp. 440 - 450
• Main Authors: Borshchevskiy, Valentin, Kovalev, Kirill, Round, Ekaterina, Efremov, Rouslan, Astashkin, Roman, Bourenkov, Gleb, Bratanov, Dmitry, Balandin, Taras, Chizhov, Igor, Baeken, Christian, Gushchin, Ivan, Kuzmin, Alexander, Alekseev, Alexey, Rogachev, Andrey, Willbold, Dieter, Engelhard, Martin, Bamberg, Ernst, Büldt, Georg, Gordeliy, Valentin
• Format: Journal Article
• Language: English
• Published: New York Nature Publishing Group US 01-05-2022; Nature Publishing Group
• Subjects: 631/535/1266; 631/57/2270/1140; Bacteriorhodopsin; Biochemistry; Biochemistry, Molecular Biology; Bioenergetics; Biological Microscopy; Biomedical and Life Sciences; Catalysis; Chains; Electrochemistry; High resolution; Hydrogen; Hydrogen Bonding; Hydrogen bonds; Life Sciences; Macromolecules; Membrane Biology; Protein Structure; Proteins; Protons; Structural Biology; Structure-function relationships; Translocation
• ISSN: 1545-9993; 1545-9985
• DOI: 10.1038/s41594-022-00762-2

Hydrogen bonds are fundamental to the structure and function of biological macromolecules and have been explored in detail. The chains of hydrogen bonds (CHBs) and low-barrier hydrogen bonds (LBHBs) were proposed to play essential roles in enzyme catalysis and proton transport. However, high-resolution structural data from CHBs and LBHBs is limited. The challenge is that their ‘visualization’ requires ultrahigh-resolution structures of the ground and functionally important intermediate states to identify proton translocation events and perform their structural assignment. Our true-atomic-resolution structures of the light-driven proton pump bacteriorhodopsin, a model in studies of proton transport, show that CHBs and LBHBs not only serve as proton pathways, but also are indispensable for long-range communications, signaling and proton storage in proteins. The complete picture of CHBs and LBHBs discloses their multifunctional roles in providing protein functions and presents a consistent picture of proton transport and storage resolving long-standing debates and controversies.
High-resolution (≤1.2 Å) structures of functional states of bacteriorhodopsin reveal the molecular mechanism for generating a membrane proton electrochemical gradient, a key event of cell bioenergetics driving ATP synthesis.