Acquirement of water-splitting ability and alteration of the charge-separation mechanism in photosynthetic reaction centers

In photosynthetic reaction centers from purple bacteria (PbRC) and the water-oxidizing enzyme, photosystem II (PSII), charge separa-tion occurs along one of the two symmetrical electron-transfer branches. Here we report the microscopic origin of the unidirec-tional charge separation, fully considering electron-hole interac-tion, electronic coupling of the pigments, and electrostatic interaction with the polarizable entire protein environments. The electronic coupling between the pair of bacteriochlorophylls is large in PbRC, forming a delocalized excited state with the lowest excitation energy (i.e., the special pair). The charge-separated state in the active branch is stabilized by uncharged polar residues in the transmembrane region and charged residues on the cyto-chrome c(2) binding surface. In contrast, the accessory chlorophyll in the D1 protein (Chl(D1)) has the lowest excitation energy in PSII. The charge-separated state involves Chl(D1)(center dot+) and is stabilized predom-inantly by charged residues near the Mn4CaO5 cluster and the pro-ceeding proton-transfer pathway. It seems likely that the acquirement of water-splitting ability makes Chl(D1) the initial elec-tron donor in PSII.