Electronic Structure and Spectroscopy of Tetranuclear Mn4O4 and CaMn3O4 Complexes as Models of the Oxygen Evolving Complex in Photosystem II

Citation

Lee, Heui Beom (2019) Electronic Structure and Spectroscopy of Tetranuclear Mn4O4 and CaMn3O4 Complexes as Models of the Oxygen Evolving Complex in Photosystem II. Dissertation (Ph.D.), California Institute of Technology. doi:10.7907/S6NR-3N42. https://resolver.caltech.edu/CaltechTHESIS:03112019-204258320

Abstract

This thesis describes a series of studies devoted toward the synthesis of model complexes that mimic aspects of structure, redox state, and spectroscopy of the oxygen evolving complex (OEC) of Photosystem II. The OEC is a unique metallocofactor featuring a heteronuclear CaMn₄ core that catalyzes water oxidation. While advances in spectroscopic and structural techniques offer an ever more detailed view of the structure of the S-state catalytic intermediates, the precise mechanism of O−O bond formation remains debated. Aspects such as (1) role of Ca²⁺, (2) the location of the substrate waters, and (3) the (electronic) structure of the S-state intermediates remain unclear. To obtain a better understanding of the OEC, systematic structure−function(property) studies on relevant model complexes may be necessary. Despite significant efforts to prepare tetra- and pentanuclear complexes as models of the OEC, relevant complexes in terms of structure, redox state, spectroscopy, and reactivity are rare, likely due to the synthetic challenges of accessing a series of isolable clusters that are suitable for comparisons.

Chapter 1 presents a survey of tetramanganese model compounds with an emphasis on redox state and electronic structure, as probed by magnetometry and EPR spectroscopy. Structurally characterized model complexes are grouped according to Mn oxidation states and the S-state that they are mirroring. In contrast to the vast number of spectroscopic studies on the OEC, studies that probe the effect of systematic changes in structure on the spectroscopy of model complexes are rare in the literature.

Chapter 2 presents ongoing synthetic efforts to prepare accurate structural models of the OEC. The synthesis of accurate structural models is hampered by the low structural symmetry of the cluster, the presence of two types of metals, and the propensity of oxo moieties to form extended oligomeric structures. Desymmetrization of the previously reported trinucleating ligand leads to the formation of tetranuclear Mn₄^II precursors. Oxidation in the presence of Ca²⁺ leads to a CaMn₄O₂ model of the OEC, underscoring the utility of low-symmetry multinucleating ligands in the synthesis of hitherto unobserved oxo-bridged multimetallic core geometries related to the OEC.

Chapter 3 presents a series of [Mn^IIIMn₃^IVO₄] cuboidal complexes as spectroscopic models of the S₂ state of the OEC. Such complexes resemble the oxidation state and EPR spectra of the S₂ state, and the effect of systematic changes in the nature of the bridging ligands on spectroscopy was studied. Results show that the electronic structure of tetranuclear Mn complexes is highly sensitive to even small geometric changes and the nature of the bridging ligands. Model studies suggest that the spectroscopic properties of the OEC may also react very sensitively to small changes in structure; the effect of protonation state and other reorganization processes needs to be carefully assessed.

Chapter 4 presents a series of [YMn₃O₄] complexes as models of the [CaMn₃O₄] subsite of the OEC. The effect of systematic changes in the basicity and chelating properties of the bridging ligands on redox potential was studied. Results show that in the absence of ligand-induced geometric distortions that enforce a contraction of metal-oxo distances, increasing the basicity of the ligands results in a decrease of cluster reduction potential. A small contraction of metal-oxo/metal-metal distances by ~0.1 Å enforced by a chelating ligand results in an increase of cluster reduction potential even in the presence of strong basic donors. Such small, protein-induced changes in Ca-oxo/Ca-Mn distances may have a similar effect in tuning the redox potential of the OEC through entatic states, and may explain the cation size dependence on the progression of the S-state cycle.

Chapter 5 presents a series of [CaMn₃O₄] and [YMn₃O₄] complexes as models of the [CaMn₃O₄] subsite of the OEC. The effect of systematic changes in cluster geometry, heterometal identity, and bridging oxo protonation on cluster spin state structure was studied. Results show that the electronic structure of the Mn₃^IV core is highly sensitive to small geometric changes, the nature of the bridging ligands, and the protonation state of the bridging oxos: the spin ground states of essentially isostructural compounds can be S = 3/2, 5/2, or 9/2. Interpretation of EPR signals and subsequent structural assignments based on an S = 9/2 spin state of the CaMn₃O₄ subsite of the OEC must be done very cautiously.

While unfinished, appendices 1 and 2 present other important aspect in OEC model chemistry. Appendix 1 presents the synthesis of ¹⁷O-labeled [Mn^IIIMn₃^IVO₄] and [CaMn₃^IVO₄] complexes as models of the OEC. Ongoing characterization of μ³-oxos in such complexes provide valuable benchmarking parameters for future mechanistic studies. Appendix 2 presents the synthesis and characterization of [Mn₄^IVO₄] cuboidal complexes as spectroscopic models of the S₃ state of the OEC, the last observable intermediate prior to O−O bond formation at the OEC.

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