The catalytic production of oxygen (O₂) in Photosystem II (PSII) involves the Mn4CaO5/6 cluster in the oxygen-evolving complex (OEC), which progresses through a series of five states (S₀-S₄). The high reactivity of the transient S₄ state is attributed to the formation of the Mn(IV)-oxyl entity. The presence of the oxyl ligand facilitates O-O bond formation via the oxyl-oxo coupling mechanism, after which oxygen evolution occurs easily.
While observations demonstrate that the S₄ state should have an open-cubane structure, there are reports showing the possibility of an S₄ state with a closed-cubane structure. Whether the S₄ state of the closed-cubane is reactive enough toward O₂ evolution has been a subject of several studies. It has been reported that the active species in the S₄ state of the closed-cubane is a Mn4(V)-oxo species, in which Mn4 adopts a five-coordinate species with a trigonal bipyramidal geometry. As a result, if such an S₄ structure is reactive, it should drive the O-O bond formation through oxo-oxo coupling rather than oxyl-oxo coupling. This hypothesis was evaluated computationally by Guo et al., who reported that for oxo-oxo coupling to take place in the closed-cubane system with a low activation barrier, a water molecule needs to coordinate to the Mn4 atom. However, in a subsequent study, Song et al. demonstrated that the coordination of an extra water molecule to the five-coordinate Mn4(V)-oxo fragment alters the electronic identity of the complex, transforming it into an Mn4(IV)-oxyl species.
We expanded this research field and addressed some key questions left unanswered in this regard using chemical quantum methods, including: What mechanism drives the transformation of the oxo ligand into the oxyl ligand? And how does the incoming ligand facilitate the formation of such reactive key species?
We found that for the Mn4(V)-oxo in the S₄ state of the closed-cubane to become activated toward O-O coupling, it needs to change its geometry from trigonal bipyramidal to square pyramidal. This structural transition considerably stabilizes the Mn4 dxy orbital, enabling an electron to transfer from the oxo ligand to the dxy orbital, converting the oxo ligand into an oxyl ligand. Although the formation of the oxyl ligand sets the stage for an easy O-O coupling process, the resulting S₄ complex with a square pyramidal structure for the Mn4 fragment lies much higher in energy than that with a trigonal bipyramidal structure, making the overall barrier for O-O coupling relatively energy demanding.
However, it should be noted that the Mn4 fragment with a square pyramidal structure has an empty site for coordination. In this situation, a water molecule can coordinate to this empty site, stabilizing the S₄ state with square pyramidal geometry for Mn4. This stabilization reduces the energy gap between the Mn(V)-oxo and Mn(IV)-oxyl species, significantly lowering the overall activation barrier for oxyl-oxo coupling.