Models of the Oxygen-Evolving Complex of Photosystem II

In the five chapters that follow, I delineate my efforts over the last five years to synthesize structurally and chemically relevant models of the Oxygen Evolving Complex (OEC) of Photosystem II. The OEC is nature’s only water oxidation catalyst, in that it forms the dioxygen in our atmosphere necessary for oxygenic life. Therefore understanding its structure and function is of deep fundamental interest and could provide design elements for artificial photosynthesis and manmade water oxidation catalysts. Synthetic endeavors towards OEC mimics have been an active area of research since the mid 1970s and have mutually evolved alongside biochemical and spectroscopic studies, affording ever-refined proposals for the structure of the OEC and the mechanism of water oxidation. This research has culminated in the most recent proposal: a low symmetry Mn₄CaO₅ cluster with a distorted Mn₃CaO₄ cubane bridged to a fourth, dangling Mn. To give context for how my graduate work fits into this rich history of OEC research, Chapter 1 provides a historical timeline of proposals for OEC structure, emphasizing the role that synthetic Mn and MnCa clusters have played, and ending with our Mn₃CaO₄ heterometallic cubane complexes.

In Chapter 2, the triarylbenzene ligand framework used throughout my work is introduced, and trinuclear clusters of Mn, Co, and Ni are discussed. The ligand scaffold consistently coordinates three metals in close proximity while leaving coordination sites open for further modification through ancillary ligand binding. The ligands coordinated could be varied, with a range of carboxylates and some less coordinating anions studied. These complexes’ structures, magnetic behavior, and redox properties are discussed.

Chapter 3 explores the redox chemistry of the trimanganese system more thoroughly in the presence of a fourth Mn equivalent, finding a range of oxidation states and oxide incorporation dependent on oxidant, solvent, and Mn salt. Oxidation states from Mn^II₄ to Mn^IIIMn^IV₃ were observed, with 1-4 O^2– ligands incorporated, modeling the photoactivation of the OEC. These complexes were studied by X-ray diffraction, EPR, XAS, magnetometry, and CV.

As Ca²⁺ is a necessary component of the OEC, Chapter 4 discusses synthetic strategies for making highly structurally accurate models of the OEC containing both Mn and Ca in the Mn₃CaO₄ cubane + dangling Mn geometry. Structural and electrochemical characterization of the first Mn₃CaO₄ heterometallic cubane complex— and comparison to an all-Mn Mn₄O₄ analog—suggests a role for Ca²⁺ in the OEC. Modification of the Mn₃CaO₄ system by ligand substitution affords low symmetry Mn₃CaO₄ complexes that are the most accurate models of the OEC to date.

Finally, in Chapter 5 the reactivity of the Mn₃CaO₄ cubane complexes toward O- atom transfer is discussed. The metal M strongly affects the reactivity. The mechanisms of O-atom transfer and water incorporation from and into Mn₄O₄ and Mn₄O₃ clusters, respectively, are studied through computation and ¹⁸O-labeling studies. The μ3-oxos of the Mn₄O₄ system prove fluxional, lending support for proposals of O^2– fluxionality within the OEC.

Transition metal clusters supported by multinucleating ligand frameworks as models of biological active sites

This dissertation describes efforts to model biological active sites with small molecule clusters. The approach used took advantage of a multinucleating ligand to control the structure and nuclearity of the product complexes, allowing the study of many different homo- and heterometallic clusters. Chapter 2 describes the synthesis of the multinucleating hexapyridyl trialkoxy ligand used throughout this thesis and the synthesis of trinuclear first row transition metal complexes supported by this framework, with an emphasis on tricopper systems as models of biological multicopper oxidases. The magnetic susceptibility of these complexes were studied, and a linear relation was found between the Cu-O(alkoxide)-Cu angles and the antiferromagnetic coupling between copper centers. The triiron(II) and trizinc(II) complexes of the ligand were also isolated and structurally characterized.

Chapter 3 describes the synthesis of a series of heterometallic tetranuclear manganese dioxido complexes with various incorporated apical redox-inactive metal cations (M = Na⁺, Ca²⁺, Sr²⁺, Zn²⁺, Y³⁺). Chapter 4 presents the synthesis of heterometallic trimanganese(IV) tetraoxido complexes structurally related to the CaMn₃ subsite of the oxygen-evolving complex (OEC) of Photosystem II. The reduction potentials of these complexes were studied, and it was found that each isostructural series displays a linear correlation between the reduction potentials and the Lewis acidities of the incorporated redox-inactive metals. The slopes of the plotted lines for both the dioxido and tetraoxido clusters are the same, suggesting a more general relationship between the electrochemical potentials of heterometallic manganese oxido clusters and their “spectator” cations. Additionally, these studies suggest that Ca²⁺ plays a role in modulating the redox potential of the OEC for water oxidation.

Chapter 5 presents studies of the effects of the redox-inactive metals on the reactivities of the heterometallic manganese complexes discussed in Chapters 3 and 4. Oxygen atom transfer from the clusters to phosphines is studied; although the reactivity is kinetically controlled in the tetraoxido clusters, the dioxido clusters with more Lewis acidic metal ions (Y³⁺ vs. Ca²⁺) appear to be more reactive. Investigations of hydrogen atom transfer and electron transfer rates are also discussed.

Appendix A describes the synthesis, and metallation reactions of a new dinucleating bis(N-heterocyclic carbene)ligand framework. Dicopper(I) and dicobalt(II) complexes of this ligand were prepared and structurally characterized. A dinickel(I) dichloride complex was synthesized, reduced, and found to activate carbon dioxide. Appendix B describes preliminary efforts to desymmetrize the manganese oxido clusters via functionalization of the basal multinucleating ligand used in the preceding sections of this dissertation. Finally, Appendix C presents some partially characterized side products and unexpected structures that were isolated throughout the course of these studies.

Synthetic, structural and mechanistic studies of interactions of carbon, nitrogen, and oxygen nucleophiles with bis-pentamethylcyclopentadienyl zirconium and hafnium derivatives

The reactivity of permethylzirconocene and permethylhafnocene complexes with various nucleophiles has been investigated. Permethylzirconocene reacts with sterically hindered ketenes and allenes to afford metallacycle products. Reaction of these cummulenes with permethylzirconocene hydride complexes affords enolate and σ-allyl species, respectively. Reactions which afford enolate products are nonstereospecific, whereas reactions which afford allyl products initially give a cis-σ-allyl complex which rearranges to its trans isomer. The mechanism of these reactions is proposed to occur either by a Lewis Acid-Lewis Base interaction (ketenes) or by formation of a π-olefin intermediate (allenes).

Permethylzirconocene haloacyl complexes react with strong bases such as lithium diisopropylamide or methylene trimethylphosphorane to afford ketene compounds. Depending on the size of the alkyl ketene substituent, the hydrogenation of these compounds affords enolate-hydride products with varying degrees of stereoselectivity. The larger the substituent, the greater is the selectivity for cis hydrogenation products.

The reaction of permethylzirconocene dihydride and permethylhafnocene dihydride with methylene trimethylphosphorane affords methyl-hydride and dimethyl derivatives. Under appropriate conditions, the metallated-ylide complex 1, (η^5-C_5(CH_3)_5)_2 Zr(H)CH_2PMe_2CH_2, is also obtained and has been structurally characterized by X-ray diffraction techniques. Reaction of 1 with CO affords (η^5-C_5(CH_3)_5)_2 Zr(C,O-η^2 -(PMe_3)HC=CO)H which exists in solution as an equilibrium mixture of isomers. In one isomer (2), the η^2-acyl oxygen atom occupies a lateral equatorial coordination position about zirconium, whereas in the other isomer (3), the η-acyl oxygen atom occupies the central equatorial position. The equilibrium kinetics of the 2→3 isomerization have been studied and the structures of both complexes confirmed by X-ray diffraction methods. These studies suggest a mechanism for CO insertion into metal-carbon bonds of the early transition metals.

Permethylhafnocene dihydride and permethylzirconocene hydride complexes react with diazoalkanes to afford η^2-N, N' -hydrazonido species in which the terminal nitrogen atom of the diazoalkane molecule has inserted into a metal-hydride or metal-carbon bond. The structure of one of these compounds, Cp*_2Zr(NMeNCTol_2)OH, has been determined by X-ray diffraction techniques. Under appropriate conditions, the hydrazonido-hydride complexes react with a second equivalent of diazoalkene to afford η' -N-hydrazonido-η^2-N, N' -hydrazonido species.