Oxidation of the Non-Heme Iron Complex in Photosystem II^†

In photosystem II (PSII), the redox properties of the non-heme iron complex (Fe complex) are sensitive to the redox state of quinones (Q_A/B), which may relate to the electron/proton transfer. We calculated the redox potentials for one-electron oxidation of the Fe complex in PSII [E_m(Fe)] based on the reference value E_m(Fe) = +400 mV at pH 7 in the Q_A⁰Q_B⁰ state, considering the protein environment in atomic detail and the associated changes in protonation pattern. Our model yields the pH dependence of E_m(Fe) with −60 mV/pH as observed in experimental redox titration. We observed significant deprotonation at D1-Glu244 in the hydrophilic loop region upon Fe complex oxidation. The calculated pK_a value for D1-Glu244 depends on the Fe complex redox state, yielding a pK_a of 7.5 and 5.5 for Fe²⁺ and Fe³⁺, respectively. To account for the pH dependence of E_m(Fe), a model involving not only D1-Glu244 but also the other titratable residues (five Glu in the D-de loops and six basic residues near the Fe complex) seems to be needed, implying the existence of a network of residues serving as an internal proton reservoir. Reduction of Q_A/B yields +302 mV and +268 mV for E_m(Fe) in the Q_A^-Q_B⁰ and Q_A⁰Q_B^- states, respectively. Upon formation of the Q_A⁰Q_B^- state, D1-His252 becomes protonated. Forming Fe³⁺Q_BH₂ by a proton-coupled electron transfer process from the initial state Fe²⁺Q_B^- results in deprotonation of D1-His252. The two EPR signals observed at g = 1.82 and g = 1.9 in the Fe²⁺Q_A^- state of PSII may be attributed to D1-His252 with variable and fixed protonation, respectively.