Proc.NatlAcad.Sci.USAhttp://doi.org/38b(2015)

Credit: © 2015 NAS

The mechanism of the photosynthetic oxidation of water has proven difficult to elucidate. The formation of dioxygen from water is known to take place at the active site of the photosystem II enzyme — dubbed the oxygen-evolving complex (pictured) — which comprises a Mn4CaO5 cluster. This cluster's highest oxidation state is thought to promote O–O bond formation, but it has remained challenging to characterize this species. Two mechanisms have been proposed for water oxidation and they both involve a high-valent manganese centre with a terminal oxido ligand. This moiety is thought to be either a Mn(IV)-oxyl radical or a Mn(V)-oxo species. Now, based on the combined experimental and theoretical study of three synthetic model compounds, a team of researchers led by Andrew Borovik at the University of California, Irvine, supports the involvement of a Mn(V)-oxo state.

The researchers prepared a mononuclear model that approximately mimics the Mn atoms at the centre of the oxygen-evolving complex; they used a trianionic ureaylate-based ligand (H3buea3−) that favours local C3 symmetry around the manganese and provides an intramolecular hydrogen-bonding network. A Mn(III) complex was initially prepared and oxidized — with either one or two equivalents of ferrocenium — in order to better understand the properties of the model at higher oxidation states. This gave a series of three complexes that were each characterized by a combination of X-ray absorption and electron paramagnetic resonance spectroscopy methods, as well as being analysed using density functional theory.

All three complexes adopt similar, high-spin mononuclear structures with the expected trigonal bipyramidal coordination geometry. Their molecular and electronic structures — including the covalent character of the Mn–O bonds and the spin density on the oxido ligand — concurred towards a Mn(III), a Mn(IV), and a Mn(V) complex, and provided no evidence for the presence a Mn(IV)-oxyl radical species. This means that the oxidation of Mn(III) occurs sequentially at the manganese centre, rather than at the ligand, and suggest that a high-spin Mn(V)-oxo moiety, similar to that seen in this study, may be at play in photosynthetic water oxidation.