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 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 Mn-1 and Mn-4 of two electrons from the reactant oxos, O-5 and O-6, resulting in an unoccupied antibonding sigma(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 A which may explain the relatively short O-5-O-6 bond distance reported in experimental structure studies. Alternatively the short O-5-O-6 bond distance may reflect a dynamic equilibrium model across the whole O-O potential energy surface.