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 S₁ state, as well as in the reduced S₀ and oxidized S₂ 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 Å 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; η² 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.