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

Quantum chemical calculations are described which rationalize the recent X-ray diffraction (XRD) structure at 2.25 Å of the Mn₄ Ca 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 Mn^III ions being present in all metastable S states.