Redox Potential of the Oxygen-Evolving Complex in the Electron Transfer Cascade of Photosystem II

In photosystem II (PSII), water oxidation occurs in the Mn₄CaO₅ cluster with the release of electrons via the redox-active tyrosine (TyrZ) to the reaction-center chlorophylls (P_D1/P_D2). Using a quantum mechanical/molecular mechanical approach, we report the redox potentials (E_m) of these cofactors in the PSII protein environment. The E_m values suggest that the Mn₄CaO₅ cluster, TyrZ, and P_D1/P_D2 form a downhill electron transfer pathway. E_m for the first oxidation step, E_m(S₀/S₁), is uniquely low (730 mV) and is ∼100 mV lower than that for the second oxidation step, E_m(S₁/S₂) (830 mV) only when the O4 site of the Mn₄CaO₅ cluster is protonated in S₀. The O4-water chain, which directly forms a low-barrier H-bond with the Mn₄CaO₅ cluster and mediates proton-coupled electron transfer in the S₀ to S₁ transition, explains why the second lowest oxidation state, S₁, is the most stable and S₀ is converted to S₁ even in the dark.