QM/MM models of the O2-evolving complex of photosystem II

This paper introduces structural models of the oxygen-evolving complex of photosystem II (PSII) in the dark-stable S-1 state, as well as in the reduced S-0 and oxidized S-2 states, with complete ligation of the metal-oxo cluster by amino acid residues, water, hydroxide, and chloride. The models are developed according to state-of-the-art quantum mechanics/molecular mechanics (QM/MM) hybrid methods, applied in conjunction with the X-ray crystal structure of PSII from the cyanobacterium Thermosynechococcus elongatus, recently reported at 3.5 angstrom resolution. Manganese and calcium ions are ligated consistently with standard coordination chemistry assumptions, supported by biochemical and spectroscopic data. Furthermore, the calcium-bound chloride ligand is found to be bound in a position consistent with pulsed electron paramagnetic resonance data obtained from acetate-substituted PSII. The ligation of protein ligands includes monodentate coordination of D1-D342, CP43-E354, and D1-D170 to Mn(1), Mn(3), and Mn(4), respectively; A2 coordination of D1-E333 to both Mn(3) and Mn( 2); and ligation of D1-E189 and D1-H332 to Mn(2). The resulting QM/MM structural models are consistent with available mechanistic data and also are compatible with X-ray diffraction models and extended X-ray absorption fine structure measurements of PSII. It is, therefore, conjectured that the proposed QM/MM models are particularly relevant to the development and validation of catalytic water-oxidation intermediates.