Mechanism of a high free-energy transduction efficiency of Bacillus PS3 F1-ATPase from the perspective of solvent entropy

Abstract

Bacillus PS3 F1-ATPase is a rotary molecular motor with a 100% free-energy transduction efficiency (The 100% efficiency means that the free-energy change upon hydrolysis of adenosine triphosphate (ATP) is almost completely consumed by the external dissipation arising from the rotation of the central stalk (γ subunit) of F1-ATPase.). In this work, to elucidate the mechanism of 100% free-energy transduction efficiency, the rotation of Bacillus PS3 F1-ATPase was investigated from the perspective of solvent entropy. The two F1-ATPase structures of the catalytic- and binding-dwell states recently published were used to compute the solvation entropy (The γ subunit of the F1-ATPase structure at the binding-dwell state is rotated by 44° relative to the structure of the catalytic-dwell state). To compute the solvation entropy, the integral equation theory was used. It was found that the change in the solvent entropy of the F1-ATPase upon 44° rotation of the γ subunit is approximately zero, which is surprising because a large structural change occurs in F1-ATPase upon rotation. The present result indicated the compensation of solvent entropy in the F1-ATPase. The compensation behavior was discussed by decomposing the solvent entropy of F1-ATPase into the components of the solvent entropy of subunits and that at the interfaces between the adjacent subunits. We also discussed that the system energy and conformational entropy would also remain unchanged upon the 44° rotation of the γ subunit. Based on the results and discussion, the following rotation mechanism was proposed: the free energy of Bacillus PS3 F1-ATPase is unchanged upon rotation; and the ATP binding, hydrolysis of ATP, and release of products lead to the rotation. This mechanism is consistent with the 100% free-energy transduction efficiency of F1-ATPase.