The oxygen-evolving complex (OEC) is a Mn4O5Ca cluster embedded in the Photosystem II (PSII) protein complex. As the site of water oxidation, the OEC is connected to the lumen by channels that conduct water, oxygen, and/or protons during the catalytic cycle. The hydrogen-bond networks found in these channels also serve to stabilize the oxidized intermediates, known as the S states. We review recent developments in characterizing these networks via protein mutations, molecular inhibitors, and computational modeling. On the basis of these results, we highlight regions of the PSII protein in which changes have indirect effects on the S1, S2, and S3 oxidation states of the OEC while still allowing photosynthetic activity.

Photosynthetic water oxidation occurs at the oxygen-evolving complex (OEC) of Photosystem II (PSII). The OEC, which contains a Mn4CaO5 inorganic cluster ligated by oxides, waters and amino-acid residues, cycles through five redox intermediates known as S(i) states (i = 0-4). The electronic and structural properties of the transient S4 intermediate that forms the O-O bond are not well understood. In order to gain insight into how water is activated for O-O bond formation in the S4 intermediate, we have performed a detailed analysis of S-state dependent substrate water binding kinetics taking into consideration data from Mn coordination complexes. This analysis supports a model in which the substrate waters are both bound as terminal ligands and react via a water-nucleophile attack mechanism.

The biomimetic oxomanganese complex [Mn III/IV 2 (μ-O) 2 (terpy) 2 (OH 2 ) 2 ](NO 3 ) 3 (1; terpy = 2,2′:6′,2″-terpyridine) catalyzes O 2 evolution from water when activated by oxidants, such as oxone (2KHSO 5 • KHSO 4 •K 2 SO 4 ). The mechanism of this reaction has never been characterized, due to the fleeting nature of the intermediates. In the present study, we elucidate the underlying reaction mechanism through experimental and theoretical analyses of competitive kinetic oxygen isotope effects (KIEs) during catalytic turnover conditions. The experimental 18 O KIE is a sensitive probe of the highest transition state in the O 2 -evolution mechanism and provides a strict constraint for calculated mechanisms. The 18 O kinetic isotope effect of 1.013 ± 0.003 measured using natural abundance reactants is consistent with the calculated isotope effect of peroxymonosulfate binding to the complex, as described by density functional theory (DFT). This provides strong evidence for peroxymonosulfate binding being both the first irreversible and rate-determining step during turnover, in contrast to the previously held assumption that formation of a high-valent Mn-oxo/oxyl species is the highest barrier step that controls the rate of O 2 evolution by this complex. The comparison of the measured and calculated KIEs supplements previous kinetic studies, enabling us to describe the complete mechanism of O 2 evolution, starting from when the oxidant first binds to the manganese complex to when O 2 is released. The reported findings lay the groundwork for understanding O 2 evolution catalyzed by other biomimetic oxomanganese complexes, with features common to those of the O 2 -evolving complex of photosystem II, providing experimental and theoretical diagnostics of oxygen isotope effects that could reveal the nature of elusive reaction intermediates.

The S redox intermediate of the oxygen-evolving complex in photosystem II is present as two spin isomers. The S = 1/2 isomer gives rise to a multiline electron paramagnetic resonance (EPR) signal at g = 2.0, whereas the S = 5/2 isomer exhibits a broad EPR signal at g = 4.1. The electronic structures of these isomers are known, but their role in the catalytic cycle of water oxidation remains unclear. We show that formation of the S = 1/2 state from the S = 5/2 state is exergonic at temperatures above 160 K. However, the S = 1/2 isomer decays to S more slowly than the S = 5/2 isomer. These differences support the hypotheses that the S state is formed via the S state S = 5/2 isomer and that the stabilized S state S = 1/2 isomer plays a role in minimizing SQ decay under light-limiting conditions.