Theoretical Evaluation of Structural Models of the S₂ State in the Oxygen Evolving Complex of Photosystem II: Protonation States and Magnetic Interactions

Abstract

Protonation states of water ligands and oxo bridges are intimately involved in tuning the electronic structures and oxidation potentials of the oxygen evolving complex (OEC) in Photosystem II, steering the mechanistic pathway, which involves at least five redox state intermediates S(n) (n = 0-4) resulting in the oxidation of water to molecular oxygen. Although protons are practically invisible in protein crystallography, their effects on the electronic structure and magnetic properties of metal active sites can be probed using spectroscopy. With the twin purpose of aiding the interpretation of the complex electron paramagnetic resonance (EPR) spectroscopic data of the OEC and of improving the view of the cluster at the atomic level, a complete set of protonation configurations for the S(2) state of the OEC were investigated, and their distinctive effects on magnetic properties of the cluster were evaluated. The most recent X-ray structure of Photosystem II at 1.9 Å resolution was used and refined to obtain the optimum structure for the Mn(4)O(5)Ca core within the protein pocket. Employing this model, a set of 26 structures was constructed that tested various protonation scenarios of the water ligands and oxo bridges. Our results suggest that one of the two water molecules that are proposed to coordinate the outer Mn ion (Mn(A)) of the cluster is deprotonated in the S(2) state, as this leads to optimal experimental agreement, reproducing the correct ground state spin multiplicity (S = 1/2), spin expectation values, and EXAFS-derived metal-metal distances. Deprotonation of Ca(2+)-bound water molecules is strongly disfavored in the S(2) state, but dissociation of one of the two water ligands appears to be facile. The computed isotropic hyperfine couplings presented here allow distinctions between models to be made and call into question the assumption that the largest coupling is always attributable to Mn(III). The present results impose limits for the total charge and the proton configuration of the OEC in the S(2) state, with implications for the cascade of events in the Kok cycle and for the water splitting mechanism.

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

“…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.…”

An Institutional Approach to Solar Fuels Research

“…[11][12][13][14][15] Other aspects that can still be learned from the biological systems are, for example, the efficient coupling of electron and proton transfer and the optimal geometry and electronic structure for O-O bond formation. Therefore, a tight interplay between researchers working on the biological processes and those developing man-made devices will contribute significantly to a faster development and implementation of devices for artificial photosynthesis.…”

“…One of the more successful areas is solar energy related research. This research covers projects involving the synthesis and application of nanomaterials such as carbon nanotubes [16][17][18] ; the production of organic optoelectronic devices [19][20][21] ; synthesis of industrial catalysts [22][23][24] ; fundamental studies on the mechanism of enzymes (such as photosystem II) [9,11,[25][26][27] ; elucidation of the genome sequence, metabolism and biomass formation of various species [28][29][30] ; combustion, gasification and torrefaction of biomass including ash behaviour [31][32][33][34][35][36][37] ; the improvement of biomass (wood) quantity and quality by breeding and genetic modification [38,39] ; and implementation of a biorefinery concept at industrial scale. [40][41][42][43][44][45] For building and maintaining these research facilities and efforts, internal and external funding is required.…”

“…2) connects 15 group leaders that cover the fields of plant physiology and natural photosynthesis (including photosynthetic water-splitting), catalysis, photochemistry, spectroscopy, crystallography, nanomaterials, physics, mathematics, and device-building. The approach is two-fold: (a) understanding and improving natural photosynthesis, [9,11,[25][26][27] and (b) applying this knowledge to the construction of low cost, printable artificial membranes for the direct (wireless) conversion of solar energy into fuels. [12,66] This environment is led by the author.…”