Biological dioxygen generation occurs within Photosystem II (PSII) in cyanobacteria and plants. The active site responsible for this transformation, the Oxygen Evolving Complex (OEC), consists of a Mn4CaOn cluster embedded in a large protein complex. Given the broad fundamental interest and potential applications of water splitting to make dioxygen, the structure of this cluster and the mechanism of catalysis have been the subject of many spectroscopic, computational, synthetic, crystallographic and biochemical studies. Despite significant advances, the mechanism of oxygen production is still not well understood. The exact Mn oxidation states along the catalytic cycle and the site of O-O bond formation continue to be debated. The large protein matrix has complicated direct studies of the OEC active site and the synthesis of accurate small-molecule models has been hampered by the complexity of the cluster. Our goals include developing synthetic routes to MnxMOn models (x=3, 4;M=Ca, Mn, other metals) of the OEC and undertaking mechanistic studies that will allow a deeper understanding of the effects different constituents (metals, ancillary and oxo ligands, protonation state) have on the chemical and physical properties of the cluster relevant to achieving high oxidation states and effecting O2 production. To that end, we will test hypotheses regarding electron, oxygen-atom and proton transfers and ligand substitution in these complex systems with implications for the assembly of the clusters and O-O bond formation. With few exceptions, the synthesis of predictable manganese oxide clusters has been frustrated by the propensity of oxo ligands to bridge and form complicated oligomeric structures. Our approach to overcoming this problem is to use relatively small, but rigid organic frameworks to support trimanganese complexes that have been elaborated to site-differentiated metal-oxo clusters, including a Mn3CaO4 moiety. These structural models will allow for spectroscopic benchmarking (EPR, XES, XAS) in comparison with the biological system. Our work on synthetic complexes will complement the studies performed on the protein by allowing systematic structure- reactivity studies to uncover the chemical features that control the properties of these clusters and the mechanism of catalysis.
This application is relevant to the NIH mission as it addresses questions related to the biological function of metals. Our goals are to test mechanistic hypotheses related to the function of Photosystem II from plants by investigating model metal-oxo clusters and to determine the chemical principles underlying the biological production of dioxygen. The described electron, proton and oxygen-atom transfer studies are relevant to many such processes occurring at metal sites in proteins of living organisms, including humans.