Tetranuclear CaMn₃O₄ and Mn₄O₄ Complexes as Spectroscopic Models of the Oxygen Evolving Complex of Photosystem II

Citation

Shiau, Angela Ann (2023) Tetranuclear CaMn₃O₄ and Mn₄O₄ Complexes as Spectroscopic Models of the Oxygen Evolving Complex of Photosystem II. Dissertation (Ph.D.), California Institute of Technology. doi:10.7907/hdx3-fe49. https://resolver.caltech.edu/CaltechTHESIS:06012023-232619718

Abstract

This thesis describes a series of studies focused on tetranuclear model complexes of the Oxygen Evolving Complex (OEC) of Photosystem II (PSII). The OEC is a unique CaMn₄O₄ metallocofactor responsible for biological water oxidation, producing the dioxygen in the atmosphere required for aerobic life. Advances in spectroscopic and structural studies have deepened our understanding of the mechanism and S-state intermediates of the OEC, but details regarding the (1) role of Ca²⁺, (2) location of substrate waters, (3) (electronic) structures of the S-states, and (4) precise mechanism of the O−O bond formation remain debated. It is proposed that synthetic model complexes, due to tunability in aspects such as metal composition, oxidation state, geometry, and ligand environment, can provide important structure-function and structure-property relationships applicable to the OEC. However, due to synthetic challenges, series of complexes suitable for such comparisons remain rare in the literature.

In Chapter 1, a brief introduction to the OEC and recent advances in the characterization of the S-state intermediates is discussed. Relationships between synthetic model complexes and how they influence mechanistic proposals for the biological system are highlighted. While it is clear spin state and cluster geometry are strongly correlated, it is important to also consider the effects of smaller, systematic changes in structure and ligand environment on the spectroscopic properties of multimetallic model complexes.

Chapter 2 presents a magnetometry and spectroscopic study of a series of related CaMn^IV₃O₄ complexes varying in the symmetry of the cluster core, ligand environment, and protonation state of the bridging oxo groups. These complexes serve as models of the CaMn^IV₃ cuboidal subsite, where cluster spin state has been previously proposed to be indicative of cluster geometry. Results from our study show that intact CaMn^IV₃O₄ cubane structures can possess spin states of S = 3/2, 5/2, and 9/2, with spin state changes attributed to minor distortions within the cluster core and, importantly, from protonation state of bridging oxo moieties. Thus, interpretation of and structural assignments based on the assumption of a S = 9/2 CaMn^IV₃O₄ subsite must be done cautiously.

Chapter 3 presents a series of Mn^IIIMn^IV₃ cuboidal complexes as spectroscopic models of the S₂ state of the OEC. Though not in the same geometric arrangement of Mn ions as in the OEC, these model complexes bear remarkably similar EPR spectroscopic features to the low-spin multiline signal of the S₂ state. Importantly, differences within this series of essentially isostructural complexes emphasize how the electronic structures of tetranuclear Mn complexes are highly sensitive to changes in ligand environment. Specifically, the energy gap between the ground S = 1/2 spin state and higher spin excited states can be tuned based on ligand electronics, resulting in complexes where both high-spin and low-spin features can be observed by EPR spectroscopy.

In Chapter 4, we expand upon our previous series of Mn^IIIMn^IV₃ model complexes utilizing a new synthetic approach to access complexes varying in Mn coordination numbers of five and six. Importantly, both proposed structures of the S₂ state contain a five-coordinate Mn^III poised for binding an additional aquo or hydroxide ligand in the S₂ to S₃ transition. Results from this study demonstrate that Mn coordination number can significantly affect the spin state and observed spectroscopy of tetramanganese-oxo clusters. The complex featuring a five coordinate Mn^III possesses a ground spin state of S_G = 5/2 and reactivity with water generates a Mn^IIIMn^IV₃O₄ complex with all pseudo-octahedral Mn centers displaying a S = 1/2 ground state.

Chapter 5 details ligand design strategies in accessing higher oxidation state clusters beyond Mn^IIIMn^IV₃. The S₃-state is the last observable intermediate prior to O−O bond formation and assigned as S = 3. Previous studies from our group demonstrated the first synthetic example corroborating this spin state, concurrent with a change from antiferromagnetic coupling within the cluster core to overall ferromagnetic coupling upon oxidation to the Mn^IV₄ oxidation state. Synthetic challenges remain in accessing related, isolable clusters. Utilizing aspects of ligand charge and basicity of a disiloxide ligand, a room temperature stable Mn^IV₄O₄ cluster was isolated and studied via magnetometry and EPR spectroscopy. Results provide a second example of a MnIV4 cluster assigned as S = 3.

While unfinished, Appendix 1 presents spectroscopic studies of model Mn^IIIMn^IV₃ complexes putatively bound to biologically relevant substrates such as water, hydroxide, methanol, and ammonia. Such chemical alterations and the spectroscopic effects arising from them have been widely studied in the biological system, providing information on the electronic structure of the OEC as well as, importantly, ruling out potential substrate water binding sites. As reactivity with small molecules typically requires an open-coordination site, such studies have been rare in the literature due to the difficulty in accessing lower-coordinate Mn sites within multimetallic Mn clusters. Thus, the ongoing characterization of these reaction products are proposed to be invaluable as benchmarking tools for future mechanistic work.