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 Mn ₄CaO ₅ 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 Mn ₄CaO ₅ 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.