Tetranuclear [Mn III Mn 3 IV O 4 ] Complexes as Spectroscopic Models of the S 2 State of the Oxygen Evolving Complex in Photosystem II

• Published in: Journal of the American Chemical Society Vol. 140; no. 49; pp. 17175 - 17187
• Main Authors: Lee, Heui Beom, Shiau, Angela A, Oyala, Paul H, Marchiori, David A, Gul, Sheraz, Chatterjee, Ruchira, Yano, Junko, Britt, R David, Agapie, Theodor
• Format: Journal Article
• Language: English
• Published: United States 12-12-2018
• Subjects: Biomimetic Materials - chemical synthesis; Biomimetic Materials - chemistry; Coordination Complexes - chemical synthesis; Coordination Complexes - chemistry; Electrochemistry; Electron Spin Resonance Spectroscopy; Magnetic Phenomena; Manganese - chemistry; Molecular Structure; Oxidation-Reduction; Oxygen - chemistry; Photosystem II Protein Complex - chemistry; Temperature
• ISSN: 0002-7863; 1520-5126
• DOI: 10.1021/jacs.8b09961

Despite extensive biochemical, spectroscopic, and computational studies, the mechanism of biological water oxidation by the oxygen evolving complex (OEC) of Photosystem II remains a subject of significant debate. Mechanistic proposals are guided by the characterization of reaction intermediates such as the S
state, which features two characteristic EPR signals at g = 2 and g = 4.1. Two nearly isoenergetic structural isomers have been proposed as the source of these distinct signals, but relevant structure-electronic structure studies remain rare. Herein, we report the synthesis, crystal structure, electrochemistry, XAS, magnetic susceptibility, variable temperature CW-EPR, and pulse EPR data for a series of [Mn
Mn
O
] cuboidal complexes as spectroscopic models of the S
state of the OEC. Resembling the oxidation state and EPR spectra of the S
state of the OEC, these model complexes show two EPR signals, a broad low field signal and a multiline signal, that are remarkably similar to the biological system. The effect of systematic changes in the nature of the bridging ligands on spectroscopy were 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. Our 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 need to be carefully assessed.