Simulation and modeling of the Rhodobacter sphaeroides bacterial reaction center II:: Primary charge separation

This paper is focused on the molecular dynamics modeling of the primary charge separation in the photosynthetic reaction center (RC) of Rhodobacter sphaeroides. The kinetic parameters for the electron transfer along the active (L) and inactive (M) sides were obtained from a long MD trajectory, 3.4 ns, of the RC in an amphophilic environment made of detergent and water. Both nuclear and electronic polarizations are explicitly included in our calculation. With no postprocessing parameter fit, our modeling computes, for two different charge distributions, the driving forces for the transfer of an excess electron to B-L and H-L from P*, in good agreement with experiments. The multiexponential kinetics of the primary charge separation is also predicted, consistent with experimentally observed kinetics. The decay of the P* state is composed of four characteristic times due to both the conformational heterogeneity of the protein and the two possible mechanisms, superexchange and sequential. At room temperature, the latter is favored over superexchange with decay rates close to experimental rates. Nevertheless, the proximity between the computed diabatic free-energy surfaces on the L side yields a superexchange electronic coupling matrix element very near its resonance point and, thus, very sensitive to changes in the driving forces. For variations of at most 1.3 kcal mol(-1), smaller than the accuracy of our theoretical approach, superexchange might be favored over the two-step mechanism. Finally, our molecular modeling strongly indicates that the position of the diabatic freeenergy surfaces for the primary charge separation cannot by itself account for the directionality of the primary charge separation. A strong electrostatic potential around the special pair that favors the polarization of the transferring electron toward regions closer to B-L than to B-M is found. This polarization could significantly increase the electronic coupling between P* and B-L, thus accounting, at least in part, for the directionality of the electron transfer.