Torque generation through the random movement of an asymmetric rotor: A potential rotational mechanism of the γ subunit of F(1)-ATPase.

Abstract

The rotation of the γ subunit of F(1)-ATPase is stochastic, processive, unidirectional, reversible through an external torque, and stepwise with a slow rotation. We propose a mechanism that can explain these properties of the rotary molecular motor, and that can determine the direction of rotation. The asymmetric structures of the γ subunit, both at the tip of the shaft (C and N termini) and at the part (ε subunit) protruding from the α(3)β(3) subunits, are critical. The torque required for stochastic rotation is generated from the impulsive reactive force due to the random collisions between the γ subunit and the quasihexagonal α(3)β(3) subunits. The rotation is the result of the random motion of the confined asymmetric γ subunit. The steps originate from the chemical reactions of the γ subunit and physical interaction between the γ subunit and the flexible protrusions of the α(3)β(3) subunits. An external torque as well as a configurational modification in the γ subunit (the central rotor) can reverse the rotational direction. We demonstrate the applicability of the mechanism to a macroscopic simulation system, which has the essential ingredients of the F(1)-ATPase structure, by reproducing the dynamic properties of the rotation.