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 PD1/PD2 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 PD1/PD2 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 PD1 and 1141–1201 mV for PD2, depending on the protonation state of the Mn4CaO5 cluster. The results showed that E m(PD1) was lower than E m(PD2), favoring localization of the charge of the cationic state more on PD1. The PD1 •+/PD2 •+ charge ratio determined by the large-scale QM/MM calculations with the explicit PSII protein environment yielded a PD1 •+/PD2 •+ 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(PD1)/E m(PD2) 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 PD1 •+ population than PD2 •+ appears to be an inevitable fate of the intact PSII that possesses water oxidation activity.