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Light-driven oxidation of water to dioxygen in plants, algae, and cyanobacteria is catalyzed within photosystem II (PS II) by a Mn 4Ca cluster. Although the cluster has been studied by many different methods, its structure and mechanism have remained elusive. X-ray absorption and emission spectroscopy and extended X-ray absorption fine structure studies have been particularly useful in probing the electronic and geometric structures and the mechanism of the water oxidation reaction. Recent progress, reviewed here, includes polarized X-ray absorption spectroscopy measurements of PS II single crystals. Analysis of those results has constrained the Mn 4Ca cluster geometry to a set of three similar high-resolution structures. The structure of the cluster from the present study is unlike either the 3.0- or 3.5-A-resolution X-ray structures or other previously proposed models. The differences between the models derived from X-ray spectroscopy and crystallography are predominantly because of damage to the Mn 4Ca cluster by X-rays under conditions used for the structure determination by X-ray crystallography. X-ray spectroscopy studies are also used for studying the changes in the structure of the Mn 4Ca catalytic center as it cycles through the five intermediate states known as the S i states ( i = 0-4). The electronic structure of the Mn 4Ca cluster has been studied more recently using resonant inelastic X-ray scattering spectroscopy (RIXS), in addition to the earlier X-ray absorption and emission spectroscopy methods. These studies are revealing that the assignment of formal oxidation states is overly simplistic. A more accurate description should consider the charge density on the Mn atoms, which includes the covalency of the bonds and delocalization of the charge over the cluster. The geometric and electronic structures of the Mn 4Ca cluster in the S states derived from X-ray spectroscopy are leading to a detailed understanding of the mechanism of O-O bond formation during the photosynthetic water-splitting process.

Where Water Is Oxidized to Dioxygen: Structure of the Photosynthetic Mn4Ca Cluster from X-ray Spectroscopy

Where Water Is Oxidized to Dioxygen: Structure of the Photosynthetic Mn₄Ca Cluster from X-ray Spectroscopy