Oxygen-Evolving Mn Cluster in Photosystem II: The Protonation Pattern and Oxidation State in the High-Resolution Crystal Structure

Abstract

Extensive quantum chemical DFT calculations were performed on the high-resolution (1.9 Å) crystal structure of photosystem II in order to determine the protonation pattern and the oxidation states of the oxygen-evolving Mn cluster. First, our data suggest that the experimental structure is not in the S(1)-state. Second, a rather complete set of possible protonation patterns is studied, resulting in very few alternative protonation patterns whose relevance is discussed. Finally, we show that the experimental structure is a mixture of states containing highly reduced forms, with the largest contribution (almost 60%) from the S(-3)-state, Mn(II,II,III,III).

Quantum mechanics/molecular mechanics simulation of the ligand vibrations of the water-oxidizing Mn 4 CaO 5 cluster in photosystem II

“…Most of these simulations focused on the geometry and the spin properties of the Mn 4 CaO 5 cluster to reproduce the X-ray structure as well as EXAFS and EPR data (10,13,15,20,21). In a recent study, Chuah et al (23) performed DFT calculations on the Mn 4 CaO 5 cluster with its firstshell ligands to outline how carboxylate stretching frequencies behave on Mn oxidation and deprotonation.…”

“…The S 2 /S 1 difference spectrum of a Ca-depleted WOC (28) was also simulated. These FTIR spectra show subtle changes in bond lengths and interactions of carboxylate groups, thus providing a different way of evaluating the most accurate WOC model from previous simulations using EXAFS and EPR data (10,13,15,20,21). This QM/MM simulation provides sufficient reproduction of the FTIR spectra, showing the significance of carboxylate ligands in the water oxidation mechanism.…”

“…Calculations using the density functional theory (DFT) and quantum mechanics/molecular mechanics (QM/MM) methods can be used to predict individual S-state structures and hence, the reaction scheme. Experimental data, such as EPR and extended X-ray absorption fine structure (EXAFS), as well as X-ray structural information were simulated using these methods to identify the protonation structure and the oxidation states (10,13,15,20,21), although a definite conclusion has not yet been reached.In contrast to EPR and EXAFS, which provide information mainly about the Mn 4 CaO 5 core, FTIR spectroscopy provides structural information about the protein moiety and water molecules coupled to the Mn 4 CaO 5 cluster (25-27). FTIR spectroscopy, which detects molecular vibrations, is highly sensitive to the structures and interactions of functional groups, and hence, the FTIR difference technique can recognize subtle structural changes at a much finer structural resolution than X-ray crystallography.…”

“…With the information of atomic coordinates from high-resolution X-ray structures of the WOC, quantum chemical calculation is now a very powerful method in investigation of the water oxidation mechanism (10,(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24). Calculations using the density functional theory (DFT) and quantum mechanics/molecular mechanics (QM/MM) methods can be used to predict individual S-state structures and hence, the reaction scheme.…”

“…Calculations using the density functional theory (DFT) and quantum mechanics/molecular mechanics (QM/MM) methods can be used to predict individual S-state structures and hence, the reaction scheme. Experimental data, such as EPR and extended X-ray absorption fine structure (EXAFS), as well as X-ray structural information were simulated using these methods to identify the protonation structure and the oxidation states (10,13,15,20,21), although a definite conclusion has not yet been reached.…”