Nonadiabatic one-electron transfer mechanism for the O–O bond formation in the oxygen-evolving complex of photosystem II

Highlights: • New O–O bond formation mechanism of photosystem II oxygen-evolving complex is proposed. • At least five reaction steps were required in the S4 to S0 transition. • Initial proton transfer requires a highest activation barrier among the five reaction steps. • O–O single bond is formed by a nonadiabatic one-electron transfer from the Mn cluster to Yz. • Proton transfer occurs to neutralize the Yz anion. The reaction mechanism of the O₂ formation in the S₄ state of the oxygen-evolving complex of photosystem II was clarified at the quantum mechanics/molecular mechanics (QM/MM) level. After the Yz (Y161) oxidation and the following proton transfer in the S₃ state, five reaction steps are required to produce the molecular dioxygen. The highest barrier step is the first proton transfer reaction (0 → 1). The following reactions involving electron transfers were precisely analyzed in terms of their energies, structures and spin densities. We found that the one-electron transfer from the Mn₄Ca cluster to Y161 triggers the O–O sigma bond formation.