Distribution of the Cationic State over the Chlorophyll Pair of the Photosystem II Reaction Center

The reaction center chlorophylls a (Chla) of photosystem II (PSII) are composed of six Chla molecules including the special pair Chla P_D1/P_D2 harbored by the D1/D2 heterodimer. They serve as the ultimate electron abstractors for water oxidation in the oxygen-evolving Mn₄CaO₅ cluster. Using the PSII crystal structure analyzed at 1.9 Å resolution, the redox potentials of P_D1/P_D2 for one-electron oxidation (E_m) were calculated by considering all PSII subunits and the protonation pattern of all titratable residues. The E_m(Chla) values were calculated to be 1015–1132 mV for P_D1 and 1141–1201 mV for P_D2, depending on the protonation state of the Mn₄CaO₅ cluster. The results showed that E_m(P_D1) was lower than E_m(P_D2), favoring localization of the charge of the cationic state more on P_D1. The P_D1^•+/P_D2^•+ charge ratio determined by the large-scale QM/MM calculations with the explicit PSII protein environment yielded a P_D1^•+/P_D2^•+ ratio of ∼80/∼20, which was found to be due to the asymmetry in electrostatic characters of several conserved D1/D2 residue pairs that cause the E_m(P_D1)/E_m(P_D2) difference, e.g., D1-Asn181/D2-Arg180, D1-Asn298/D2-Arg294, D1-Asp61/D2-His61, D1-Glu189/D2-Phe188, and D1-Asp170/D2-Phe169. The larger P_D1^•+ population than P_D2^•+ appears to be an inevitable fate of the intact PSII that possesses water oxidation activity.