Mechanism by which a single water molecule affects primary charge separation kinetics in a bacterial photosynthetic reaction center of Rhodobacter sphaeroides

Abstract

Using quantum-chemical methods, we have studied the role played by water molecules W-A and W-B that are bound by hydrogen bonds to accessory bacteriochlorophyll molecules BA and BB in the process of primary charge separation in the reaction center of Rhodobacter Sphaeroides. We have found that the occurrence of a rotational mode of the W-A molecule at 32 cm−1 and/or its harmonics in stimulated emission of an electron donor P* and the dynamics of population of the states P+BA− and P+HA− may be related to the structural heterogeneity of the reaction center and the existence of a conformation in which the W-A molecule is predominantly involved in one hydrogen bond (with BA). Based on the calculated redox potentials BA and P, it has been shown that the appearance of the W-A molecule in the reaction center reduces the energy of the P+BA− state by ∼600 cm−1. This is somewhat smaller than the influence of the amino-acid residue TyrM210 (∼870 cm−1) and correlates well with a substantial decrease in the electron transfer rate in mutant forms of reaction centers GM203L (which do not contain W-A molecules) and YM210F (in which TyrM210 is replaced with Phe). The data obtained allow us to suggest that rotation of the water molecule with a fixed position of its H atom that is involved in a hydrogen bond with the keto carbonyl group of BA is initiated due to the charge separation between the halves of special pair P and the formation of the state PA+PB−. The large effect of this rotation on the kinetics of population of the states P+BA− and P+HA− after the excitation of P is quite consistent with its influence on the energy of the state P+BA−.