Mechanism of Water Splitting by Photosystem II

Abstract

The light driven water splitting achieved in the oxygen evolving complex (OEC) of Photosystem II is a critical process that sustains our biosphere. Photosynthetic water splitting is fascinating in its complexity, inspiring due to its practical applications in designing artificial photosynthesis, and not yet understood. At the heart of the water splitting process is the Mn4Ca cluster embedded in a fine tuned protein environment.The electronic structure and geometry of this cluster were probed by X-ray spectroscopy at the functional room temperature state.1, 2 Detailed kinetic analysis of the X-ray induced damage was performed and allowed selection of undamaging conditions for experimentation. High-quality extended X-ray absorption fine structure (EXAFS) spectra of the OEC at room temperature will be presented and compared with XRD and DFT derived molecular models of the dark stable S1 state. The determined Debye-Waller factors, sensitive to dynamic processes, support the rigid structure of the Mn4Ca cluster at room temperature.Laser-pump X-ray probe time-resolved X-ray emission measurements (XES) allowed monitoring of changes in the electronic structure of the OEC in real time during the catalysis. Using time-resolved XES we monitored the evolution of the electronic structure of the OEC of Photosystem II during the most critical S3 to S0 transition which results in O2 evolution. Our data show no oxidation but only a gradual reduction of the Mn centers after excitation of the complex past the S3 state. These observations allow us to propose a unique O-O bond formation and water splitting mechanism. Combined with DFT modeling, our analysis reveals the mechanism of catalytic water splitting.1. Davis et al. J. Phys. Chem. B 117, 9161-9169 (2013).2. Davis et al. J. Phys. Chem. Lett. 3, 1858-1864 (2012).