Dynamic evolution of S0–S3 at the oxygen-evolving complex with spin markers under photoelectric polarization

Water oxidation at the oxygen-evolving complex (OEC) of the photosystem II is catalyzed by the core cluster CaMn₄O₅, which has been projected to experience five intermediate states Sᵢ in the Kok's cycle since the 1970s. However, the detailed dynamics of state evolutions still remains unclear, albeit with the general fact that the process is initiated by the transfer of photoelectrons with the steady electron donors of the water molecules. Based on density-functional simulations, we find that the spin flips of manganese atoms between the consecutive states in the electric polarization field can be used as a marker to uncover the intricate dynamic evolutions and the underlying dynamics. The dynamic electron and proton transfers and water insertion and dissociation are traced to reveal the evolution pathways of S₀--S₃ with commensurate spin flips towards the exact spin configuration of the next state. In particular, the various water insertions and dissociations at coordination sites of the S₂ open and closed cubane isomers are predicted with constraints on the necessary spin flips. Our study paves the way to uncover the animated OEC evolutions with the spin flips that await more experimental verifications and lays a solid ground for revealing the mechanism of dioxygen generation via the pending S₄ state.