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 S3 state. Concerted electron flow between the Mn4O5 and Mn1O6 bonds of the complex and the nascent O-O bond is monitored using intrinsic bond orbital analysis along the reaction path. Concerted transfer to Mn1 and Mn4 of two electrons from the reactant oxos, O5 and O6, resulting in an unoccupied antibonding σ2p* 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.