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

Abstract

In photosynthetic reaction centers from purple bacteria (PbRC) and the water-oxidizing enzyme, photosystem II (PSII), charge separation occurs along one of the two symmetrical electron-transfer branches. Here we report the microscopic origin of the unidirectional charge separation, fully considering electron-hole interaction, 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 cytochrome <i>c</i>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^•+ and is stabilized predominantly by charged residues near the Mn₄CaO₅ cluster and the proceeding proton-transfer pathway. It seems likely that the acquirement of water-splitting ability makes Chl_D1 the initial electron donor in PSII.