Kinetic Asymmetry and Directionality of Nonequilibrium Molecular Systems

Abstract

Scientists have long been fascinated by the biomolecular machines in living systems that process energy and information to sustain life. The first synthetic molecular rotor capable of performing repeated 360° rotations due to a combination of photo‐ and thermally activated processes was reported in 1999. The progress in designing different molecular machines in the intervening years has been remarkable, with several outstanding examples appearing in the last few years. Despite the synthetic accomplishments, there remains confusion regarding the fundamental design principles by which the motions of molecules can be controlled, with significant intellectual tension between mechanical and chemical ways of thinking about and describing molecular machines. A thermodynamically consistent analysis of the kinetics of several molecular rotors and pumps shows that while light driven rotors operate by a power‐stroke mechanism, kinetic asymmetry—the relative heights of energy barriers—is the sole determinant of the directionality of catalysis driven machines. Power‐strokes—the relative depths of energy wells—play no role whatsoever in determining the sign of the directionality. These results, elaborated using trajectory thermodynamics and the nonequilibrium pump equality, show that kinetic asymmetry governs the response of many non‐equilibrium chemical phenomena.

From Brownian to Deterministic Motor Movement in a DNA-Based Molecular Rotor

“…There have been various attempts to implement synthetic Brownian motors in physical and chemical systems, e.g., using optically trapped microparticles, , microfluidic systems, or synthetic molecular motors driven by light . It has been noted, however, that externally driven systems behave fundamentally different than chemically driven molecular machines, the latter of which are constrained by the principle of microscopic reversibility. , …”

“…Our results show that a Brownian motor can be generated from a DNA-based nanodevice without explicit design by simply utilizing irregularities in its potential landscape. One of the major challenges for future work will be realization of out-of-equilibrium systems by other means, in particular Brownian motors that are fueled by chemical reactions. , The working principle of chemically driven molecular machines is fundamentally different from the externally driven system shown here, however, as they have to be able to “gate” a chemical reaction depending on their current mechanical state. , …”

“…20 It has been noted, however, that externally driven systems behave fundamentally different than chemically driven molecular machines, the latter of which are constrained by the principle of microscopic reversibility. 21,22 Recently, the DNA origami technique 23−25 was utilized to create a DNA-based rotary device with explicitly designed ratchet-like obstacles. 26 In this study, the origami rotor was driven out of equilibrium using an electrical field, whose direction was periodically switched from one direction to its opposite (i.e., by 180°) and back.…”

“…32,33 The working principle of chemically driven molecular machines is fundamentally different from the externally driven system shown here, however, as they have to be able to "gate" a chemical reaction depending on their current mechanical state. 21,22 ■ ASSOCIATED CONTENT…”

Analysis of kinetic asymmetry in a multi-cycle chemical reaction network establishes the principles for autonomous compartmentalized molecular ratchets

“…[33,36] Such an autonomous operation mechanism was previously described in detail exclusively in relation to light-driven systems, [37][38][39] and, as a result, the theoretical basis for such a mechanism remains unexplored in relation to ground-state reactivity. [40] Here, we present the treatment of kinetic asymmetry in an epitomic multi-cycle network. In particular, we focused on a redox-powered network, mapping closely the one underlying the recently reported autonomous electrically driven system, to investigate the origin of its somewhat unconventional ratchet mechanism.…”