Evidence of O-O Bond Formation in the Final Metastable S State of Nature's Water Oxidizing Complex Implying a Novel Mechanism of Water Oxidation.

A novel mechanism for the final stages of Nature's photosynthetic water oxidation to molecular oxygen is proposed. This is based on a comparison of experimental and broken symmetry density functional theory (BS-DFT) calculated geometries and magnetic resonance properties of water oxidizing complex models in the final metastable oxidation state, S. We show that peroxo models of the S state are in vastly superior agreement with the current experimental structural determinations compared with oxo-hydroxo models. Comparison of experimental and BS-DFT calculated Mn hyperfine couplings for the electron paramagnetic resonance (EPR) visible form shows better agreement for the oxo-hydroxo model. An equilibrium between oxo-hydroxo and peroxo models is proposed for the S state and the major implications for the final steps in the water oxidation mechanism are analyzed and discussed.