Characterization of Oxygen Bridged Manganese Model Complexes Using Multifrequency¹⁷O-Hyperfine EPR Spectroscopies and Density Functional Theory

Abstract

Multifrequency pulsed EPR data are reported for a series of oxygen bridged (μ-oxo/μ-hydroxo) bimetallic manganese complexes where the oxygen is labeled with the magnetically active isotope (17)O (I = 5/2). Two synthetic complexes and two biological metallocofactors are examined: a planar bis-μ-oxo bridged complex and a bent, bis-μ-oxo-μ-carboxylato bridge complex; the dimanganese catalase, which catalyzes the dismutation of H2O2 to H2O and O2, and the recently identified manganese/iron cofactor of the R2lox protein, a homologue of the small subunit of the ribonuclotide reductase enzyme (class 1c). High field (W-band) hyperfine EPR spectroscopies are demonstrated to be ideal methods to characterize the (17)O magnetic interactions, allowing a magnetic fingerprint for the bridging oxygen ligand to be developed. It is shown that the μ-oxo bridge motif displays a small positive isotropic hyperfine coupling constant of about +5 to +7 MHz and an anisotropic/dipolar coupling of -9 MHz. In addition, protonation of the bridge is correlated with an increase of the hyperfine coupling constant. Broken symmetry density functional theory is evaluated as a predictive tool for estimating hyperfine coupling of bridging species. Experimental and theoretical results provide a framework for the characterization of the oxygen bridge in Mn metallocofactor systems, including the water oxidizing cofactor of photosystem II, allowing the substrate/solvent interface to be examined throughout its catalytic cycle.

Dinuclear manganese(iii) complexes with bioinspired coordination and variable linkers showing weak exchange effects: a synthetic, structural, spectroscopic and computation study

“…1 and feature Mn⋯Mn distances ranging from 8.7 to 15.1 Å as controlled by the spacer group of the dicarboxylate. Previously reported dimanganese(III,IV) and dimanganese(II,III) systems have been investigated by HFEPR, [35][36][37] and more importantly, so have dimanganese(III) complexes, such as a μ-oxido complex by Retegan et al, 10 a μ-fluorido complex by Pedersen et al, 8 and a system more relevant to those reported here, namely a dimanganese(III,III) complex without any bridging atoms, but with covalent connections between the two Mn III ions via two trans four-bond π-conjugated O-C-C-C-O pathways. 28 A tetranuclear complex comprising a square grid of Mn III ions linked by Schiff base ligands has also been studied by HFEPR, 38 but this complicated spin system is beyond the present study.…”

Biomolecular EPR Meets NMR at High Magnetic Fields

“…The same advantages can be seen for more complex systems. Our laboratories have recently reported high field EDNMR data for a series of oxygen (µ-oxo) bridged manganese homodimers and manganese-iron heterodimers [583]. This set included two simple synthetic complexes and two biological cofactors, from the manganese calatase enzyme and R2-like ligand oxidase (R2lox) enzyme.…”

“…At this field range, the Larmor frequency, ν n , of many nuclei is significantly larger than 10 MHz, allowing for their detection by EDNMR. Over the last decade, a series of reports appeared that used high-field EDNMR to characterize a number of chemical systems and materials with a wide variety of nuclei in radical [228,236,545,[557][558][559][560][561][562][563][564] and transition metal containing systems [272,273,275,276,[565][566][567][568][569][570][571][572][573][574][575][576][577][578][579][580][581][582][583][584].…”

“…We also note that at high field, correlation transitions (those involving multiple nuclei) can be more easily suppressed that can contribute to the observed linewidth at lower microwave bands (X-, Q-band). In the text below we describe recent results from our laboratories on using EDNMR to characterize radicals and paramagnetic metal complexes at higher magnetic fields [236,273,274,545,558,559,[562][563][564]572,583]. For further information about the EDNMR method we refer the reader to recent reviews [274,585].…”

Direct detection and characterization of bioinorganic peroxo moieties in a vanadium complex by 17O solid-state NMR and density functional theory

“…Electronic properties of enzymatic oxygen centers have been most commonly probed indirectly by electron paramagnetic resonance (EPR) and electron nuclear double resonance (ENDOR) spectroscopies [6–13]. However, direct detection of 17 O centers in catalytic reaction intermediates is rare.…”