The Mechanism of Substrate Delivery and Activation in the Solar Water Oxidation Reaction of Photosystem II

Abstract

The solar water-splitting protein complex, photosystem II (PSII), catalyzes one of the most energetically demanding reactions in Nature by using light energy to drive a catalyst capable of oxidizing water. The water oxidation reaction is catalyzed by the tetramanganese-calcium-oxo (Mn4Ca-oxo) cluster in the oxygen-evolving complex (OEC) of PSII which cycles through five light-driven charge-storage or S-state intermediates (S0-S4) as it accumulates charge equivalents to split water. However, a detailed mechanism of the reaction remains elusive as it requires knowledge of the binding and activation of substrate water molecules in the higher S-state intermediates of the OEC. In particular, the binding of substrate in the S2 to S3 state transition of the OEC that leads to O-O bond formation is poorly understood because of the inability of conventional methods to probe water molecules. We are developing state-of-the-art two-dimensional (2D) hyperfine sublevel correlation spectroscopy methods for high-resolution proton crystallography of the S state intermediates of the water oxidation reaction. In this presentation, we will describe ongoing studies in our laboratory that employ small molecule analogs and site-directed mutagenesis of PSII to elucidate the mechanism of the delivery and binding of substrate water at the Mn4Ca-oxo cluster in the S2 and S3 states the the OEC. These studies have important implications on the mechanistic models for water oxidation in the OEC which is important as it is a promising blueprint for the development of artificial catalysts for water splitting that can generate clean and renewable energy from sunlight. †This study is supported by the Photosynthetic Systems Program, Office of Basic Energy Sciences, United States Department of Energy (DE-FG02-07ER15903 (KVL) and DE-FG02-05ER1564 (GWB)).