Implications of structural heterogeneity for the electronic structure of the final oxygen-evolving intermediate in photosystem II.

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 S 3 state to the transient O 2 -evolving S 4 state of the OEC. Using quantum chemical calculations, we show that each S 3 isomer leads to a different electronic structure formulation for the active S 4 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 S 4 state: this takes the form of a five-coordinate and locally high-spin (S Mn = 1) Mn(V) site. This formulation for the S 4 state evolves naturally from a preceding S 3 -state structural intermediate that contains a quasi-trigonal-bipyramidal Mn(IV) ion. The results strongly suggest that water binding in the S 3 state is not prerequisite for reaching the oxygen-evolving S 4 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 O O 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. A new possible formulation is suggested for the catalytically active S 4 state of the oxygen evolving complex in Photosystem II: it contains a high-spin five-coordinate Mn(V)-oxo entity as a result of decoupling water binding from cofactor oxidation and can support a genuine even-electron mechanism for water oxidation. Unlabelled Image • The oxygen-evolving cluster of photosystem-II exists in different structural forms. • Each S 3 isomer progresses into a distinct O 2 -evolving S 4 state. • S 3 structures with six-coordinate Mn ions form Mn(IV)-oxyl S 4 species. • Delayed water binding allows Mn-centered oxidation, forming a genuine Mn(V)-oxo in S 4. • This enables genuine four-electron nucleophilic coupling in dioxygen evolution. [ABSTRACT FROM AUTHOR]