Evidence of O–O Bond Formation in the Final Metastable S₃ State of Nature’s Water Oxidizing Complex Implying a Novel Mechanism of Water Oxidation

Abstract

A novel mechanism for the final stages of Nature's photosynthetic water oxidation to molecular oxygen is proposed. This is based on a comparison of experimental and broken symmetry density functional theory (BS-DFT) calculated geometries and magnetic resonance properties of water oxidising complex models in the final metastable oxidation state, S 3. We show that peroxo models of the S 3 state are in vastly superior agreement with the current experimental structural determinations compared with oxohydroxo models. Comparison of experimental and BS-DFT calculated 55 Mn hyperfine couplings for the EPR visible form shows better agreement for the oxo-hydroxo model. An equilibrium between oxo-hydroxo and peroxo models is proposed for the S 3 state and the major implications for the final steps in the water oxidation mechanism are analysed and discussed.

The S3 State of the Oxygen-Evolving Complex: Overview of Spectroscopy and XFEL Crystallography with a Critical Evaluation of Early-Onset Models for O–O Bond Formation

“…These two forms were previously discussed by Krewald et al [30], who had concluded that the presence or absence of the O6H-O5 hydrogen bond has only a small energetic effect and does not significantly perturb the magnetic and spectroscopic properties of the cluster [30]. The same conclusions are reached by Corry and O'Malley [50]. Note that the O5-O6 distance is ca.…”

“…The proton of the OH group may either point towards the O5 bridge or away from it, establishing instead a hydrogen bond with another acceptor group, for example the carboxylate of Glu189. In either case, the distance between O5 and O6 is computed at ~2.4-2.6 Å [30,[48][49][50]68]. According to DFT calculations these alternative hydrogen-bonding patterns lie too close to be reliably distinguishable energetically [30].…”

“…[30], the experimentally observed pattern of two large and two small 55 Mn hyperfine coupling constants can be reproduced by an oxo-hydroxo structural model (see associated spin projection coefficients in Figure 4c [30,68]), even though the smaller values are overestimated compared to experiment. Computationally derived structures with different bonding and magnetic topologies or with alternative oxidation states do not reproduce the magnitude and distribution of the experimental 55 Mn hyperfine coupling constants as successfully [30,50,101]. Table 1.…”

“…A study by Corry and O'Malley [50] also investigated peroxo formation in the S 3 state and provided a comprehensive report of computed EPR parameters for such models. Starting from the Suga et al coordinates [46], Corry and O'Malley optimized a series of peroxo and oxo-hydroxo 229-atom models of the S 3 state with the BP86 functional, assuming a high-spin configuration in each model; properties were computed with the hybrid meta-GGA (10% HF exchange) TPSSh functional [142].…”

“…One development was the emergence of the first crystallographic models of the S 3 state resulting from X-ray free-electron laser (XFEL) studies: these models suggested that two oxygen atoms within the cluster were within bonding distance [46] or, at least, within a distance considerably shorter than that of a hydrogen bond [47]. The second development was the suggestion by a number of computational studies of the S 3 state [48][49][50][51][52] that peroxo or superoxo redox isomers (in which some Mn ions are reduced compared to the S 2 state) can be energetically accessible or even more favorable than redox isomers in which the Mn ions are oxidized with respect to the S 2 state, suggesting that early-onset O-O bond formation is feasible.…”