Rationalizing the Geometries of the Water Oxidising Complex in the Atomic Resolution, Nominal S₃ State Crystal Structures of Photosystem II

Abstract

We dedicate this paper to the memory of Tom Wydrzynski and Warwick Hillier, two friends and close colleagues of ours over many years at ANU. The work that Tom initiated with Johannes Messinger, then carried forward with Warwick and their collaborators, transformed our understanding of the OEC and critical aspects of its operation. Their results are remarkable, both as experimental tours de force, but also in the manner by which they define and constrain possibilities, for the system's function and mechanism. These are unique insights, which have often not been accorded the significance they deserve, in our view. Three atomic resolution crystal structures of Photosystem II, in the double flashed, nominal S 3 intermediate state of its Mn 4 Ca Water Oxidising Complex (WOC), have now been presented, at 2.25, 2.35 and 2.08 Å resolution. Although very similar overall, the S 3 structures differ within the WOC catalytic site. The 2.25 Å structure contains only one oxy species (O5) in the WOC cavity, weakly associated with Mn centres, similar to that in the earlier 1.95 Å S 1 structure. The 2.35 Å structure shows two such species (O5, O6), with the Mn centres and O5 positioned as in the 2.25 Å structure and O5À O6 separation of~1.5 Å. 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 O5À Ox separation < 2.1 Å. 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 Å 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 À ) positioned as in the 2.25 Å structure, and the other with the metals similarly placed, but with O5 (as H 2 O) located in the O6 position of the 2.35 Å structure. The 2.35 Å two flashed structure was likely a crystal superposition of two such forms. Here we show, by similar computational analysis, that the latest 2.08 Å S 3 structure is also a likely superposition of forms, but with O5 (as OH À ) 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.

Biomimicking Hydrogen-Bonding Network by Ammoniated and Hydrated Manganese (II) Phosphate for Electrocatalytic Water Oxidation

“…Water molecules and these amino acid residues are connected to the CaMn4O5 cluster by hydrogen bonds, which can not only stabilize the structure of the CaMn4O5 cluster, but also play an important role in OER process 35 . Bonded water molecules can provide initial reactants, facilitating rapid reactions 36 . The surrounding amino acid residues facilitate the transfer of protons and electrons in the OER process and speed up the reaction rate 35 .…”

The Nature of the Short Oxygen–Oxygen Distance in the Mn4CaO6 Complex of Photosystem II Crystals

“…20 Theoretical studies by Petrie et al proposed two possible binding positions of O5 in S 3 , one of which corresponds to O6. 21 Here we identify the microscopic origin of the short oxygen−oxygen distances in the S 3 -XFEL structures, using a QM/MM approach in the presence of the entire PSII protein environment.…”

A Computational Study of the S2 State in the Oxygen-Evolving Complex of Photosystem II by Electron Paramagnetic Resonance Spectroscopy

“…Since Mn2 is strongly indicated from computational chemistry [ 40 ] to be the single Mn IV species present in S 2 (ground state) of the OEC in the low oxidation paradigm (LOP), the NIR excitations could result in exchange of this oxidation level with Mn1 or Mn3. The possible explanation of the ≈140 K NIR-generated signals may be the inter-valence charge transfer between Mn2 and Mn3 or Mn1, and hence there may be a possible S 2 low oxidation state pattern of III III IV III or IV III III III, respectively, as earlier assumed [ 25 , 41 , 42 , 43 , 44 , 45 , 46 , 47 ].…”