Molecular mechanism of photosynthetic oxygen evolution: A theoretical approach

Possible mechanisms for O₂ evolution in photosystem II (PSII) are studied with a semiempirical one-electron molecular orbital procedure, the extended Hückel method. The oxygen coupling is examined starting from some known inorganic complexes of manganese. Idealized geometries of four binuclear complexes (two di-μ-oxo, one tri-μ-oxo and one μ-carboxylato-di-μ-oxo) are distorted to transform into O₂-bound complexes. The computed Walsh diagrams are analyzed. For these structures the predicted oxidation to dioxygen is energetically unfavorable and would require two two-electron steps forming bound peroxide as an intermediate. An in-plane approach of two oxo ligands has a lower barrier for peroxide bond formation. Four tetranuclear Mn clusters are built combining binuclear complexes, a Mn₄O₄ cubane-like core, three (Mn₂O₂)₂(μ-O₂) "dimer of dimers" cores with μ₄,η²-O₂ bound either in or out of the Mn₄ plane formed by two parallel Mn₂O₂ units, and a "planar T" combination of two orthogonal Mn₂O₂ units with a Mn₃O₂ core and μ₃,η²-O₂ bound to three Mn atoms. The assumed pathway leading to peroxide bond formation in each of these is found to have appreciably lower energy for the (Mn₂O₂)₂(μ-O₂) and the "planar T" models with in-plane O-O approach. A slight energetic advantage is calculated in the peroxide to dioxygen step when the oxo ligands are coordinated to at least three Mn ions compared to coordination to only two Mn ions. Qualitative valence bond analysis indicates that release of symmetrically coordinated dioxygen, as in cis- and trans-μ-O₂, requires overcoming an ∼1-eV electronic barrier for formation of ground-state O₂ (triplet). The tetranuclear models are introduced into speculative mechanisms and compared with current knowledge of the photosynthetic water oxidation reaction.