Torque generation mechanism in Fo motor of ATP synthase elucidated by free-energy and Coulomb-energy landscapes along the c-ring rotation

Yukinari Kamiyama; Dan Parkin; Mitsunori Takano

doi:10.1016/j.bbrc.2023.01.085

Torque generation mechanism in F_o motor of ATP synthase elucidated by free-energy and Coulomb-energy landscapes along the c-ring rotation

Biochem Biophys Res Commun. 2023 Apr 9:651:56-61. doi: 10.1016/j.bbrc.2023.01.085. Epub 2023 Feb 3.

Authors

Yukinari Kamiyama¹, Dan Parkin², Mitsunori Takano³

Affiliations

¹ Department of Pure and Applied Physics, Graduate School of Advanced Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-Ku, Tokyo, 169-8555, Japan.
² Research Institute for Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-Ku, Tokyo, 169-8555, Japan.
³ Department of Pure and Applied Physics, Graduate School of Advanced Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-Ku, Tokyo, 169-8555, Japan; Research Institute for Science and Engineering, Waseda University, 3-4-1 Okubo, Shinjuku-Ku, Tokyo, 169-8555, Japan. Electronic address: mtkn@waseda.jp.

PMID: 36791499
DOI: 10.1016/j.bbrc.2023.01.085

Abstract

F_o portion of ATP synthase is a proton-motive rotary motor. The Coulombic attraction between the conserved acidic residues in the c-ring and the arginine in the a-subunit (aR) was early proposed to drive the c-ring rotation relative to the a-subunit, and has been actually observed in our previous molecular dynamics simulation with full atomistic description of F_o embedded in the membrane. In this study, to quantify the driving force, we conducted the umbrella sampling (US) and obtained the free-energy landscape for the c-ring rotation. We first show that the free-energy gradient toward the ATP-synthesis direction appears in the deprotonated state of cE. Using the sampled snapshots that cover a wide range of the rotational angle, we further analyzed the rotational-angle dependence of the hydration and the protonation states and obtained the Coulomb-energy landscapes with a focus on the cE-aR interaction. The results indicate that both the Coulombic solvation energy of cE and the interaction energy between cE and aR contribute to the torque generation for the c-ring rotation.

Keywords: Energy landscape; GB model; Molecular dynamics simulation; Proton motive force; Solvation; pK(a).

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adenosine Triphosphate* / chemistry
Proton-Translocating ATPases* / metabolism
Rotation
Torque

Substances

Adenosine Triphosphate
Proton-Translocating ATPases