ABSTRACT
The rotatory molecular motor of F0F1-ATP-synthase funnels the protonmotive force generated by photosynthesis or respiration into the ATP synthesis. That unique enzyme first converts the proton gradient into the rotation of the membrane-embedded F0 subunit. Next, the elastic torque is transmitted to the chemical F1 motor responsible for rotary catalysis leading to ATP synthesis and release. The evolution of understanding bioenergetics in scientific papers and textbooks can be partially traced to hot disputes among scientists attempting to explain how ATP synthase works as a marvelous molecular engine. It is an excellent example of how scientific thinking is balanced at the razor's edge of the highest respect for earlier fruits of scientific creativity and audacious willingness to solve still unsolved problems, even if it requires a revolutionary paradigm shift at the expense of a scientist' pet theory. For instance, Nobelist Paul D. Boyer was able to disregard the exaggerations of his favorite theories and incorporate the essential aspects of Peter Mitchell's chemiosmotic theory into his proposal of a binding-change mechanism for proton-driven rotary catalysis. In our research, we asked the question about the evolutionary optimization of that splendid biomolecular machine by modeling chloroplast's ATPase kinetic cycle. The optimization of the transition state parameters led to the agreement with the experimental data when we used the maximum entropy production requirement in the crucial transition connecting proton transfer to ATP synthesis. Remarkably, the single joint maximum is found for the information entropy and the transitional entropy production for that essential catalytic step. The coincident maximum ensures optimal distribution of state probabilities and entropy productions associated with transitions between functional states. The maximum is obtained for the inflection point of the ATP synthesis curve, and it is in agreement with empirical estimates about the optimal angular position for the ATP-binding transition. Thus, optimal metabolic control is achieved for maximal entropy production, suggesting a statistical interpretation of ATP synthase function's evolutionary optimization. The extent of entropy production can identify evolved dissipative pathways that facilitate biomolecular function.
