Explaining the Different Geometries of the Water Oxidising Complex in the Nominal S-3 State Crystal Structures of Photosystem II at 2.25 angstrom and 2.35 angstrom

摘要

Recently two atomic resolution crystal structures of Photosystem II, in the double flashed, nominal S-3 intermediate state of its Mn4Ca water oxidising complex (WOC), have been presented (Young et al., Nature 2016, 540, 453; Suga et al., Nature 2017, 543, 131). These structures are at 2.25 angstrom and 2.35 angstrom resolution, respectively. Although highly similar in most respects, the structures differ in a key region within the WOC catalytic site. In the 2.25 angstrom structure, one oxy species (O5) is observed within the WOC cavity, weakly associated with the Mn centres, similar to that seen earlier in the 1.95 angstrom XRD structure of the S-1 intermediate (Suga et al., Nature, 2015, 517, 99). In the 2.35 angstrom structure, two such species are seen (O5, O6), with the Mn centres and O5 positioned as in the 2.25 angstrom structure and an O5-O6 separation of similar to 1.5 angstrom, consistent with peroxo formation. This suggests O5 and O6 are substrate water derived species in this double flashed form. Recently we have presented (Petrie, et al., Chem. Phys. Chem., 2017) a large scale (220 atom) quantum chemical model of the Young et al. 2.25 angstrom structure, which quantitatively explains all significant features within the WOC region of that structure, particularly the positions of the metal centres and O5 group. Critical to this was our assumption of 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), widely assumed in the literature. Here we show that our same oxidation state model predicts two classes of energetically close S-3 structural forms, analogous to the S-1 state, one with the metal centres and O5 positioned as in the 2.25 angstrom structure, and the other with the metals similarly placed, but with O5 located in the O6 position of the 2.35 angstrom structure. We show that the Suga et al. 2.35 angstrom structure is