Early Binding of Substrate Oxygen Is Responsible for a Spectroscopically Distinct S State in Photosystem II.

The biological generation of oxygen by the oxygen-evolving complex (OEC) in photosystem II (PS II) is one of nature's most important reactions. The OEC is a MnCa cluster that has multiple Mn-O-Mn and Mn-O-Ca bridges and binds four water molecules. Previously, binding of an additional oxygen was detected in the S to S transition. Here we demonstrate that early binding of the substrate oxygen to the five-coordinate Mn center in the S state is likely responsible for the S high-spin EPR signal. Substrate binding in the Mn-OH form explains the prevalence of the high-spin S state at higher pH and its low-temperature conversion into the S state. The given interpretation was confirmed by X-ray absorption spectroscopic measurements, DFT, and broken symmetry DFT calculations of structures and magnetic properties. Structural, electronic, and spectroscopic properties of the high-spin S state model are provided and compared with the available S state models. New interpretation of the high-spin S state opens opportunity for analysis of factors controlling the oxygen substrate binding in PS II.