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Tetranuclear [MnIIIMn3IVO4] Complexes as Spectroscopic Models of the S2 State of the Oxygen Evolving Complex in Photosystem II.

ABSTRACT: 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 S2 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 [MnIIIMn3IVO4] cuboidal complexes as spectroscopic models of the S2 state of the OEC. Resembling the oxidation state and EPR spectra of the S2 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.

SUBMITTER: Lee HB

PROVIDER: S-EPMC6574184 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Tetranuclear [MnIIIMn3IVO4] Complexes as Spectroscopic Models of the S2 State of the Oxygen Evolving Complex in Photosystem II.

Lee Heui Beom HB Shiau Angela A AA Oyala Paul H PH Marchiori David A DA Gul Sheraz S Chatterjee Ruchira R Yano Junko J Britt R David RD Agapie Theodor T

Journal of the American Chemical Society 20181130 49

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 S2 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, ...[more]

PMID: 30407806

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Project description:Two structurally homologous Mn compounds in different oxidation states were studied to investigate the relative influence of oxidation state and ligand environment on Mn K-edge X-ray absorption near-edge structure (XANES) and Mn Kbeta X-ray emission spectroscopy (Kbeta XES). The two manganese compounds are the di-mu-oxo compound [L'2Mn(III)O2Mn(IV)L'2](ClO4)3, where L' is 1,10-phenanthroline (Cooper, S. R.; Calvin, M. J. Am. Chem. Soc. 1977, 99, 6623-6630) and the linear mono-mu-oxo compound [LMn(III)OMn(III)L](ClO4)2, where L- is the monoanionic N,N-bis(2-pyridylmethyl)-N'-salicylidene-1,2-diaminoethane ligand (Horner, O.; Anxolabéhère-Mallart, E.; Charlot, M. F.; Tchertanov, L.; Guilhem, J.; Mattioli, T. A.; Boussac, A.; Girerd, J.-J. Inorg. Chem. 1999, 38, 1222-1232). Preparative bulk electrolysis in acetonitrile was used to obtain higher oxidation states of the compounds: the Mn(IV)Mn(IV) species for the di-mu-oxo compound and the Mn(III)Mn(IV) and Mn(IV)Mn(IV) species for the mono-mu-oxo compound. IR, UV/vis, EPR, and EXAFS spectra were used to determine the purity and integrity of the various sample solutions. The Mn K-edge XANES spectra shift to higher energy upon oxidation when the ligand environment remains similar. However, shifts in energy are also observed when only the ligand environment is altered. This is achieved by comparing the di-mu-oxo and linear mono-mu-oxo Mn-Mn moieties in equivalent oxidation states, which represent major structural changes. The magnitude of an energy shift due to major changes in ligand environment can be as large as that of an oxidation-state change. Therefore, care must be exercised when correlating the Mn K-edge energies to manganese oxidation states without taking into account the nature of the ligand environment and the overall structure of the compound. In contrast to Mn K-edge XANES, Kbeta XES spectra show less dependence on ligand environment. The Kbeta1,3 peak energies are comparable for the di-mu-oxo and mono-mu-oxo compounds in equivalent oxidation states. The energy shifts observed due to oxidation are also similar for the two different compounds. The study of the different behavior of the XANES pre-edge and main-edge features in conjunction with Kbeta XES provides significant information about the oxidation state and character of the ligand environment of manganese atoms.

Project description:The anisotropic g and hyperfine tensors of the Mn di-micro-oxo complex, [Mn(2)(III,IV)O(2)(phen)(4)](PF(6))(3).CH(3)CN, were derived by single-crystal EPR measurements at X- and Q-band frequencies. This is the first simulation of EPR parameters from single-crystal EPR spectra for multinuclear Mn complexes, which are of importance in several metalloenzymes; one of them is the oxygen-evolving complex in photosystem II (PS II). Single-crystal [Mn(2)(III,IV)O(2)(phen)(4)](PF(6))(3).CH(3)CN EPR spectra showed distinct resolved (55)Mn hyperfine lines in all crystal orientations, unlike single-crystal EPR spectra of other Mn(2)(III,IV) di-micro-oxo bridged complexes. We measured the EPR spectra in the crystal ab- and bc-planes, and from these spectra we obtained the EPR spectra of the complex along the unique a-, b-, and c-axes of the crystal. The crystal orientation was determined by X-ray diffraction and single-crystal EXAFS (Extended X-ray Absorption Fine Structure) measurements. In this complex, the three crystallographic axes, a, b, and c, are parallel or nearly parallel to the principal molecular axes of Mn(2)(III,IV)O(2)(phen)(4) as shown in the crystallographic data by Stebler et al. (Inorg. Chem. 1986, 25, 4743). This direct relation together with the resolved hyperfine lines significantly simplified the simulation of single-crystal spectra in the three principal directions due to the reduction of free parameters and, thus, allowed us to define the magnetic g and A tensors of the molecule with a high degree of reliability. These parameters were subsequently used to generate the solution EPR spectra at both X- and Q-bands with excellent agreement. The anisotropic g and hyperfine tensors determined by the simulation of the X- and Q-band single-crystal and solution EPR spectra are as follows: g(x) = 1.9887, g(y) = 1.9957, g(z) = 1.9775, and hyperfine coupling constants are A(III)(x) = |171| G, A(III)(y) = |176| G, A(III)(z) = |129| G, A(IV)(x) = |77| G, A(IV)(y) = |74| G, A(IV)(z) = |80| G.

Dataset Information

Tetranuclear [MnIIIMn3IVO4] Complexes as Spectroscopic Models of the S2 State of the Oxygen Evolving Complex in Photosystem II.

Publications

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

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