Rationalizing the 2.25 Å Resolution Crystal Structure of the Water Oxidising Complex of Photosystem II in the S3 State

Abstract

Quantum chemical calculations are described which rationalize the recent X‐ray diffraction (XRD) structure at 2.25 Å of the Mn4Ca water oxidising complex (WOC) of photosystem II (PSII) in the S3 intermediate state. The new S3 XRD structure shows remarkable similarity to earlier atomic resolution (1.9, 1.95 Å) WOC structures in the dark stable S1 state and is inconsistent with most current proposals, from computational chemistry and other sources, regarding the Mn oxidation state levels in the WOC cluster and the nature of water substrate binding, particularly in S3. This mirrors earlier failures to rationalise the WOC geometry in the 1.9 and 1.95 Å S1 XRD structures, assuming “high” paradigm Mn oxidation models. However, we recently showed that a lower Mn oxidation assumption closely reproduces the S1 XRD structures, computationally. This same “low” Mn oxidation model, now computationally applied in S3, not only reproduces the latest 2.25 Å XRD structure but also rationalises a number of other important, experimental features of the WOC, including the metal–metal distances inferred from EXAFS studies as well as earlier S3 state XRD structures of lower resolution (4–5 Å). As found previously for S1, the WOC in the S3 state is computationally revealed to be structurally variable, consistent with some EXAFS and lower‐resolution XRD data. This is a direct consequence of at least two MnIII ions being present in all metastable S states.