Computational modelling of the water oxidising complex of Photosystem II
Creators: name: Gatt, Phillip Trethowan
Publisher: name: The Australian National University
Year: 2018
Subjects: subject: QK882.G38 2012
subject: Photosynthesis Computational simulation
subject: Oxidation
subject: Photons

description: The Water Oxidising Complex of Photosystem II, which contains an oxo-bridged CaMn{u2084} cluster, is able to split water at near thermodynamic efficiency. The WOC has been examined using many experimental techniques, the ultimate goal of which is to elucidate the chemical processes involved in water oxidation. Thus far, a wealth of data has been obtained on the geometric and oxidative properties of the Ca/Mn reaction centre; however, much of it is either inconsistent or open to interpretation. Therefore, quantum chemical methods have been employed to assist in the determination of the WOC structure and the mechanism of water oxidation. A recent DFT study examined three WOC models that are broadly consistent with the Mn ion arrangements characterised by 3.7 {u00C5}, 3.5 {u00C5}, and 2.9 {u00C5} XRD structures; the Y-, Cubane-, and Hook-arrangements, respectively. It was concluded that the three models were nearly isoenergetic, and that the definitive feature between the Mn ion arrangements was the location of Mn(4). However, these model structures used a simplified form of the WOC protein environment, thereby ignoring any constraining influence the greater protein matrix of PSII may have on the geometric and electronic properties of the Ca/Mn cluster. To address this deficiency, this study uses similar DFT methods to re-examine these model systems, but with a segment of the encapsulating protein environment included that provides the polypeptide linkage between the Mn centres. Importantly, this polypeptide linkage includes His337, a non-ligating residue that lies within hydrogen bonding distance of the {u03BC}{u2083}-oxo-bridge connecting Mn(1), Mn(2), and Mn(3). Optimised models of this extended system are compared with the truncated system to assess any significant changes in the geometric and oxidative properties of the Mn cluster. Overall, three main influences on these properties are observed. Firstly, hydrogen bonding between His337 and the {u03BC}{u2083}-oxo bridge is shown to have a profound effect on the distances between the Mn(1), Mn(2), and Mn(3) ions by altering the Mn(2) oxidation state. Secondly, water ligands bound to the Mn cluster create complex hydrogen bonding networks that interact with other Mn ligands. This affects the vectors associated with Mn(1), Mn(3), and Mn(4) as well as the Mn(4) oxidation state. Thirdly, the peptide chains introduce geometric constraints on the Mn reaction centre that energetically favours the Hook-like arrangement of the 2.9 {u00C5} XRD structure, and can also impose Hook-like features on the other structure types. Finally, the strapped system is used to rationalise the structural disparities between the two most recent Hook-like XRD structures, the 2.9 and 1.9 {u00C5} XRD structures. It is found that both of these structures can be modelled using Mn oxidation levels that are consistent with the Low Oxidation State paradigm{u00B9}, and that these two structures are, remarkably, single proton tautomers of one another. The structural disparities are found to result from changes in the Mn oxidation state assignments resulting from a proton transfer between His337 and a Mn(4)-bound oxygen species. This work highlights the importance of the His337 residue and the Jahn-Teller effect associated with high-spin d{u2074} Mn centres in the S{u2081} state presumed to be representative of the XRD structures. Mean Mn oxidation level is 3.0