Computational study of oxygen evolving complex in photosystem II

Photosystem II (PSII) of photosynthetic organisms converts light energy into chemical energy by oxidizing water to dioxygen at the Mn4CaO5 oxygen evolving complex (OEC). Extensive structural data have been collected from crystal diraction, EXAFS studies and electron paramagnetic resonance (EPR), but the protonation and Mn oxidation states are still uncertain. A high-oxidation" model assigns the S1 state to have the formal Mn oxidation level of (III-IV-IV-III), whereas the low-oxidation" model posits two additional electrons. Generally, additional protons are expected to be associated with the low-oxidation model. We first consider structural features of the S0 and S1 states using a quantum mechanics/molecular mechanics (QM/MM) method. We systematically alter the hydrogenbonding network and the protonation states of bridging and terminal oxygens and His337 to investigate how they influence Mn-Mn and Mn-O distances, relative energetics, and the internal distribution of Mn oxidation states, in both high and low-oxidation state paradigms. Optimized geometries are compared to experimental data and to results from earlier computational studies. The bridging oxygens (O1, O2, O3, O4) all need to be deprotonated (O2-) to be compatible with available structural data; while the position of O5 (bridging Mn3, Mn4 and Ca) in the XFEL structure is more consistent with an OH- under the low paradigm. We show that structures with two short Mn-Mn distances, which are sometimes argued to be diagnostic of a high oxidation state paradigm, can also arise in low oxidation-state models. We conclude that the low Mn oxidation state proposal for the OEC can closely t all of the available structural data at accessible energies in a straightforward manner. Modeling at the 4 H+ protonation level of S1 under the high paradigm predicts rearrangement of bidentate D1-Asp170 to H-bond to O5 (OH-), a geometry found in articial OEC catalysts. We then investigate the geometric and spectroscopic properties of the S2 state, using quantum chemical density functional theory calculations, focusing on the neglected low paradigm. Consistent with experiments, two interconvertible electronic spin configurations are predicted, as ground states producing multiline (S = 1=2) and broad (S = 5=2) EPR signals, for the low paradigm oxidation state (III, IV, III, III) and W2 as OH- and O5 as OH-. They have open" (S = 5=2) and closed" (S = 1=2) cubane geometries. Other energetically accessible isomers with ground spin state 7/2, 9/2, or 11/2 can be obtained through perturbations of hydrogen-bonding networks (e.g. H+ from His337 to O3 or W2), consistent with experimental observations. Calculated 55Mn hyperne tensors reveal four scalar (Fermi contact) couplings that are consistent with experiments, and calculated hyperne anisotropies reveal the severe inadequacy of the magnetic dipolar approximation for hyperne anisotropies. We conclude that the low Mn oxidation state proposal for the OEC can closely t nearly all the available structural and electronic data for S2 at accessible energies. Following S3 state under the low paradigm can produce three short Mn-Mn distances and ground state S = 3 together with two classes of HFCs, but in separate congurations. We nd the direction of Jahn-Teller axis of MnIII determines the related Mn-Mn distances and exchange coupling parameters. S4 state and O{O bond formation mechanism are studied but no pathway with suciently low barrier has been found towards peroxide formation. The rearrangement of bidentate D1-Asp170 from (Mn4, Ca) to H-bond to W1 (H2O) and Ca indicates the possible role of D1-Asp170 asa proton acceptor during the water oxidation. Finally, we examine a cobalt cubane cluster in terms of peroxide and dioxygen formations. Complete energy proles have been calculated.Ph.D.Includes bibliographical referencesby He Che