Proton-Coupled Electron Transfer during the S-State Transitions of the Oxygen-Evolving Complex of Photosystem II

The oxygen-evolving complex (OEC) of photosystem II (PSII) is a unique Mn₄O₅Ca cluster that catalyzes water oxidation via four photoactivated electron transfer steps. As the protein influence on the redox and protonation chemistry of the OEC remains an open question, we present a classical valence model of the OEC that allows the redox state of each Mn and the protonation state of bridging μ-oxos and terminal waters to remain in equilibrium with the PSII protein throughout the redox cycle. We find that the last bridging oxygen loses its proton during the transition from S₀ to S₁. Two possible S₂ states are found depending on the OEC geometry: S₂ has Mn4(IV) with a proton lost from a terminal water (W1) trapped by the nearby D1-D61 if O5 is closer to Mn4, or Mn1(IV), with partial deprotonation of D1-H337 and D1-E329 if O5 is closer to Mn1. In S₃, the OEC is Mn₄(IV) with W2 deprotonated. The estimated OEC E_ms range from +0.7 to +1.3 V, enabling oxidation by P₆₈₀⁺, the primary electron donor in PSII. In chloride-depleted PSII, the proton release increases during the S₁ to S₂ transition, leaving the OEC unable to properly advance through the water-splitting cycle.