Chemical peristalsis.

Molecules that emulate in part the remarkable capabilities of protein motors were recently chemically synthesized. A promising approach is based on physically interlocked macromolecular complexes such as rotaxanes and catenanes. Using the latter, Leigh et al. [Leigh, D. A., Wong, J. K. Y., Dehez, F. & Zerbetto, F. (2003) Nature 424, 174-179] constructed a molecular rotor in which two small rings are induced by pulses of light to move unidirectionally around a third, larger ring. The mechanism is similar to that by which a peristaltic pump operates. Unlike macroscopic peristalsis, however, in which a traveling wave forces material through a series of one-way valves, the chemical peristaltic mechanism does not directly cause the small rings to move but only alters the energetics, with the motion itself arising by thermal activation over energy barriers. Engines operating by this mechanism are "Brownian" motors. Here we describe a minimal two-state mechanism for a catenane-based molecular motor. Although fluctuations caused by equilibrium processes cannot drive directed motion, nonequilibrium fluctuations, whether generated externally or by a far-from-equilibrium chemical reaction, can drive rotation even against an external torque. We discuss a possible architecture for input and output of information and energy between the motor and its environment and give a simple expression for the maximum thermodynamic efficiency. The proposed Brownian motor mechanism is consistent with the high efficiency observed by Yasuda et al. [Yasuda, Y., Noji, H., Kinoshita, K. & Yoshida, M. (1998) Cell 93, 1117-1124] for the F(1)-ATP synthase operating as an ATP-powered molecular rotor.