LAUSR

Heterogeneity in intermediate catalytic states of the oxygen-evolving complex (OEC) of Photosystem II is known from a wide range of experimental and theoretical data, but its potential implications for the mechanism of water oxidation remain unexplored. We delineate the consequences of structural heterogeneity for the final step of the catalytic cycle by tracing the evolution of three spectroscopically relevant and structurally distinct components of the last metastable S3 state to the transient O2-evolving S4 state of the OEC. Using quantum chemical calculations, we show that each S3 isomer leads to a different electronic structure formulation for the active S4 state. Crucially, in addition to previously hypothesized Mn(IV)-oxyl species, we establish for the first time, how a genuine Mn(V)-oxo can be obtained in the catalytically active S4 state: this takes the form of a five-coordinate and locally high-spin (SMn = 1) Mn(V) site. This formulation for the S4 state evolves naturally from a preceding S3-state structural intermediate that contains a quasi-trigonal-bipyramidal Mn(IV) ion. The results strongly suggest that water binding in the S3 state is not prerequisite for reaching the oxygen-evolving S4 state of the complex, supporting the notion that both substrates are preloaded at the beginning of the catalytic cycle. This scenario allows true four-electron metal-centered hole accumulation to precede OO bond formation and hence the latter can proceed via a genuine even-electron mechanism. This can occur as intramolecular nucleophilic coupling of two oxo units synchronously with the binding of a water substrate for the next catalytic cycle.