Rationalizing The Geometries Of The Water Oxidising Complex In The Atomic Resolution, Nominal S-3 State Crystal Structures Of Photosystem Ii

Three atomic resolution crystal structures of Photosystem II, in the double flashed, nominal S-3 intermediate state of its Mn4Ca Water Oxidising Complex (WOC), have now been presented, at 2.25, 2.35 and 2.08 angstrom resolution. Although very similar overall, the S-3 structures differ within the WOC catalytic site. The 2.25 angstrom structure contains only one oxy species (O5) in the WOC cavity, weakly associated with Mn centres, similar to that in the earlier 1.95 angstrom S-1 structure. The 2.35 angstrom structure shows two such species (O5, O6), with the Mn centres and O5 positioned as in the 2.25 angstrom structure and O5-O6 separation of similar to 1.5 angstrom. In the latest S-3 variant, two oxy species are also seen (O5, Ox), with the Ox group appearing only in S-3, closely ligating one Mn, with O5-Ox separation <2.1 angstrom. The O5 and O6/Ox groups were proposed to be substrate water derived species. Recently, Petrie et al. (Chem. Phys. Chem., 2017) presented large scale Quantum Chemical modelling of the 2.25 angstrom structure, quantitatively explaining all significant features within the WOC region. This, as in our earlier studies, assumed a 'low' Mn oxidation paradigm (mean S-1 Mn oxidation level of +3.0, Petrie et al., Angew. Chem. Int. Ed., 2015), rather than a 'high' oxidation model (mean S-1 oxidation level of +3.5). In 2018 we showed (Chem. Phys. Chem., 2018) this oxidation state assumption predicted two energetically close S-3 structural forms, one with the metal centres and O5 (as OH-) positioned as in the 2.25 angstrom structure, and the other with the metals similarly placed, but with O5 (as H2O) located in the O6 position of the 2.35 angstrom structure. The 2.35 angstrom two flashed structure was likely a crystal superposition of two such forms. Here we show, by similar computational analysis, that the latest 2.08 angstrom S-3 structure is also a likely superposition of forms, but with O5 (as OH-) occupying either the O5 or Ox positions in the WOC cavity. This highlights a remarkable structural 'lability' of the WOC centre in the S-3 state, which is likely catalytically relevant to its water splitting function.