Water Deprotonation via Oxo-Bridge Hydroxylation and 18O-Exchange in Free Tetra-Manganese Oxide Clusters

One of the fundamental biological reactions, the catalytically activated water-splitting, takes place at an inorganic tetra-manganese monocalcium penta-oxygen (Mn4CaO5) cluster which together with its protein ligands forms the oxygen evolution complex (OEC) of the membrane-bound pigment–protein photosystem II (PSII) of plants, algae, and cyanobacteria. In the first step of a new hierarchical approach to probe fundamental concepts of the water-splitting reactions, we present the gas-phase preparation of an isolated tetra-manganese oxide cluster ion, Mn4O4+, as a simplified model of the OEC. Reactivity studies with D216O and H218O in a gas-phase ion trap experiment reveal the exchange of the oxygen atoms of the cluster with water oxygen atoms. This provides direct experimental evidence for the ability of Mn4O4+ to dissociate water via hydroxylation of the oxo-bridges. The rate of oxygen exchange in the free cluster agrees well with the conversion rate of substrate water to O2 in photosystem II, thus supporting the involvement of bridging oxygen atoms in this process. First-principles spin density functional theory calculations reveal the molecular mechanism of the water deprotonation and oxo-bridge exchange.