A key question for the understanding of photosynthetic water oxidation is whether the four oxidizing equivalents necessary to oxidize water to dioxygen are accumulated on the four Mn ions of the oxygen-evolving complex (OEC), or whether some ligand-centered oxidations take place before the formation and release of dioxygen during the S 3 → [S 4 ] → S 0 transition. Progress in instrumentation and flash sample preparation allowed us to apply Mn Kβ X-ray emission spectroscopy (Kβ XES) to this problem for the first time. The Kβ XES results, in combination with Mn X-ray absorption near-edge structure (XANES) and electron paramagnetic resonance (EPR) data obtained from the same set of samples, show that the S 2 → S 3 transition, in contrast to the S 0 → S 1 and S 1 → S 2 transitions, does not involve a Mn-centered oxidation. On the basis of new structural data from the S 3 -state, manganese μ-oxo bridge radical formation is proposed for the S 2 → S 3 transition, and three possible mechanisms for the O-O bond formation are presented.

A key component required for an understanding of the mechanism of the evolution of molecular oxygen by the photosynthetic oxygen-evolving complex (OEC) in photosystem II (PS II) is the knowledge of the structures of the Mn cluster in the OEC in each of its intermediate redox states, or S-states. In this paper, we report the first detailed structural characterization using Mn extended X-ray absorption fine structure (EXAFS) spectroscopy of the Mn cluster of the OEC in the S0 state, which exists immediately after the release of molecular oxygen. On the basis of the EXAFS spectroscopic results, the most likely interpretation is that one of the di-μ-oxo-bridged Mn−Mn moieties in the OEC has increased in distance from 2.7 Å in the dark-stable S1 state to 2.85 Å in the S0 state. Furthermore, curve fitting of the distance heterogeneity present in the EXAFS data from the S0 state leads to the intriguing possibility that three di-μ-oxo-bridged Mn−Mn moieties may exist in the OEC instead of the two di-μ-oxo-bridged Mn−Mn moieties that are widely used in proposed structural models for the OEC. This possibility is developed using novel structural models for the Mn cluster in the OEC which are consistent with the structural information available from EXAFS and the recent X-ray crystallographic structure of PS II at 3.8 Å resolution.