Electronic–Level View of O–O Bond Formation in Nature’s Water Oxidizing Complex

The crucial O-O bond forming step in the water oxidizing complex (WOC) of photosystem II is modeled using density functional theory calculations and compared with structural X-ray free electron laser (XFEL) determinations for the penultimate S ₃ state. Concerted electron flow between the Mn ₄O5 and Mn ₁O6 bonds of the complex and the nascent O-O bond is monitored using intrinsic bond orbital analysis along the reaction path. Concerted transfer to Mn ₁ and Mn ₄ of two electrons from the reactant oxos, O5 and O6, resulting in an unoccupied antibonding σ _2p∗ orbital is the key to low barrier O-O bond formation. The potential energy surface for O-O bond formation shows a rather broad energy minimum for the oxo-oxo form ranging from 2.4-2.0 Å which may explain the relatively short O5-O6 bond distance reported in experimental structure studies. Alternatively the short O5-O6 bond distance may reflect a dynamic equilibrium model across the whole O-O potential energy surface.