Crystal Structure of a Synthetic High-Valent Complex with an Fe₂(μ-O)₂ Diamond Core. Implications for the Core Structures of Methane Monooxygenase Intermediate Q and Ribonucleotide Reductase Intermediate X

Abstract

In our efforts to model high-valent intermediates in the oxygen activation cycles of nonheme diiron enzymes such as methane monooxygenase (MMOH-Q) and ribonucleotide reductase (RNR R2-X), we have synthesized and spectroscopically characterized a series of bis(µ-oxo)diiron(III,IV) complexes, [Fe 2 (µ-O) 2 -(L) 2 ](ClO 4 ) 3 , where L is tris(2-pyridylmethyl)amine (TPA) or its ring-alkylated derivatives. We now report the crystal structure of [Fe 2 (µ-O) 2 (5-Et 3 -TPA) 2 ](ClO 4 ) 3 (2), the first example of a structurally characterized reactive iron(IV)-oxo species, which provides accurate metrical parameters for the diamond core structure proposed for this series of complexes. Complex 2 has Fe-µ-O distances of 1.805(3) Å and 1.860(3) Å, an Fe-Fe distance of 2.683(1) Å, and an Fe-µ-O-Fe angle of 94.1(1)°. The EXAFS spectrum of 2 can be fit well with a combination of four shells: 1 O at 1.82 Å, 2-3 N at 2.03 Å, 1 Fe at 2.66 Å, and 7 C at 2.87 Å. The distances obtained are in very good agreement with the crystal structure data for 2, though the coordination numbers for the first coordination sphere are underestimated. The EXAFS spectra of MMOH-Q and RNR R2-X contain features that match well with those of 2 (except for the multi-carbon shell at 2.87 Å arising from pyridyl carbons which are absent in the enzymes), suggesting that an Fe 2 (µ-O) 2 core may be a good candidate for the core structures of the enzyme intermediates. The implications of these studies are discussed.

A synthetic precedent for the [Fe IV 2 (μ-O) 2 ] diamond core proposed for methane monooxygenase intermediate Q

“…As shown in Table 1, inclusion of a single Fe scatterer at Ϸ2.7 Å dramatically improves the quality of the EXAFS fit and provides conclusive evidence that 2b is a dinuclear complex with a short FeOFe distance. Indeed, the FeOFe distance of 2b is comparable to the value of 2.68 Å found in the crystal structure of 1c (14). Finally, as with previous EXAFS studies of Fe complexes with pyridine ligands (14,16), the fit also is improved by inclusion of an additional shell of six C atoms at 2.93 Å, accounting for the shoulder at rЈ ϭ 2.5 Å and corresponding to the pyridine ␣-carbon atoms.…”

“…Indeed, the FeOFe distance of 2b is comparable to the value of 2.68 Å found in the crystal structure of 1c (14). Finally, as with previous EXAFS studies of Fe complexes with pyridine ligands (14,16), the fit also is improved by inclusion of an additional shell of six C atoms at 2.93 Å, accounting for the shoulder at rЈ ϭ 2.5 Å and corresponding to the pyridine ␣-carbon atoms. Thus, the XAS analysis provides strong support for the formulation of 2b as…”

“…The best fit to the EXAFS data reveals a first-coordination sphere consisting of two O/N atoms at 1.78 Å and four N/O atoms at 1.97 Å (Table 1). In agreement with the more oxidized nature of the diiron(IV) complex, these distances are Ϸ0.05-Å shorter than the average values determined crystallographically for 1c (14). As shown in Table 1, inclusion of a single Fe scatterer at Ϸ2.7 Å dramatically improves the quality of the EXAFS fit and provides conclusive evidence that 2b is a dinuclear complex with a short FeOFe distance.…”

“…Density functional theory (DFT) calculations from a number of groups also support the viability of such an intermediate (7)(8)(9)(10)(11). Although several mononuclear oxoiron(IV) complexes have been structurally characterized (12), thus providing valuable information regarding the catalytic mechanism of mononuclear nonheme iron enzymes (13) 3 [L c , tris(5-ethyl-2-pyridylmethyl)amine] (1c, Scheme 1) (14). However, this complex has an Fe III Fe IV oxidation state, which is one-electron reduced relative to that of MMO-Q.…”

An Fe IV O complex of a tetradentate tripodal nonheme ligand

“…Synthetic efforts in the past 10 years have demonstrated the accessibility of the iron(IV) oxidation state in a nonheme ligand environment, particularly in coupled iron(III)iron(IV) complexes (12)(13)(14)(15)(16)(17)(18); indeed one of these, [Fe 2 ( -O) 2 (5-Et 3 -tris(2-pyridylmethyl)amine, TPA) 2 ](ClO 4 ) 3 , has been crystallographically characterized (19). However, only recently has evidence for synthetic mononuclear iron(IV)-oxo species been obtained.…”