Detailed Spectroscopic and Theoretical Studies on [Fe(EDTA)(O₂)]^3-:  Electronic Structure of the Side-on Ferric−Peroxide Bond and Its Relevance to Reactivity

Abstract

A spectroscopic study of the Fe(III)-EDTA-peroxide complex using electron paramagnetic resonance (EPR), low-temperature absorption (LT-ABS), variable-temperature-variable-field (VTVH) magnetic circular dichroism (MCD), and resonance Raman (rR) spectroscopies is reported. Density functional (DFT) and INDO/ S-CI molecular orbital (MO) calculations are used to derive an experimentally calibrated bonding scheme. The molecule is described as a 6-coordinate, mononuclear, high-spin ferric-peroxide complex with a side-on η 2 -FeO 2 arrangement. EPR spectroscopy shows that the zero-field splitting (ZFS) is negative with D ) -1.0 ( 0.25 cm -1 and E/D ) 0.21. MCD and LT-ABS spectroscopies lead to the identification of at least six excited states below 35 000 cm -1 . The lowest two are assigned as ligand field sextetfquartet transitions, and the remaining transitions have peroxide to iron ligand-to-metal charge transfer (LMCT) character. The polarization of the LMCT bands in the principal axis system of the D-tensor are derived by VTVH-MCD spectroscopy. The Fe-O and O-O stretching vibrations are observed at 459 and 816 cm -1 , respectively. rR excitation profiles are simulated to obtain excited-state distortions. The weak CT bands in the visible region mainly enhance the O-O stretch, whereas the UV band dominantly enhances the metal-ligand stretch and only weakly the O-O stretch. A normal coordinate analysis shows little mechanical coupling between the two stretches and gives force constants of 3.02 mdyn/Å for the O-O stretch and 1.56 mdyn/Å for the Fe-O stretch. MO calculations show that the bonding is dominated by a strong, covalent σ-bond formed between the Fe-d xy and peroxide-π σ / orbitals with little contributions from πor δ-symmetry iron-peroxide interactions. A back-bonding interaction between Fe-3d and the peroxide-σ*-orbital that contributes to the weak O-O bond in oxyhemocyanin is not present in the Fe(III)-EDTA-peroxide complex. A calculation of the D-tensor from the INDO/S-CIS(D) wave functions gives good agreement with the experimental values and defines the orientation of the D-tensor in the molecular coordinate system. This allows the polarizations obtained from VTVH-MCD spectroscopy to be related to a molecular axis system and assists in band assignments. The negative D-value and the observed excited distortions are explained by the extensive anisotropic covalency of the FeO 2 σ-bond. Possible contributions of the electronic structure to the reactivity of non-heme iron enzymes are considered, and protonation of the peroxide ligand is proposed to lead to highly reactive species.

Hydrogen Peroxide Dependent cis-Dihydroxylation of Benzoate by Fully Oxidized Benzoate 1,2-Dioxygenase

“…The isomer shift is 0.50 mm/s, which is typical for N and O type ligands from the protein or solvent. These parameters are similar to those of the resting enzyme and unlike those of models for Fe(III)-peroxo complexes (29,36). This suggests that the model for BZDO O in which H 2 O 2 binds near but not to the iron is more likely to be correct.…”

Finding Intermediates in the O2 Activation Pathways of Non-Heme Iron Oxygenases

“…Interestingly, EPR and Mössbauer spectra with similar parameters and negative zero-field splitting have been observed for Fe(III)-peroxo model complexes. 12,28 Thus, it seems likely that the activated oxygen species of the Rieske dioxygenases is a similar peroxo adduct, although the slightly smaller isomer shift (δ = 0.5 mm/s vs 0.64 mm/s in the models) suggest that it is protonated. It was detected by forcing the formation of the species in a form of the enzyme that does not readily exchange small molecules or substrates in the normal cycle.…”

End-On and Side-On Peroxo Derivatives of Non-Heme Iron Complexes with Pentadentate Ligands: Models for Putative Intermediates in Biological Iron/Dioxygen Chemistry

“…38,71 A similar inertness has been noted for [Fe(EDTA)(η 2 -O 2 )] 3-. 39 A sideon peroxoiron(III) species has been postulated in the mechanism of arene cis-dihydroxylation by the Rieske dioxygenases 4, 74 and recently observed in the crystal structure of a ternary enzyme-substrate-O 2 complex of naphthalene dioxygenase. 5b If such a species were to be involved in the enzyme mechanism, the lack of oxidative reactivity of corresponding biomimetic complexes suggests that such a species may require subsequent activation, perhaps by protonation, to effect substrate oxidation, as also proposed for heme enzymes.…”

“…38 The only other established (η 2 -peroxo)iron complexes prior to these studies are those of Fe III (EDTA) 39 and Fe III (porphyrin). 40 The existence of an acid-base equilibrium affording low-spin Fe III -η 1 -OOH and high-spin Fe III -η 2 -O 2 species in one ligand system provides a unique opportunity to investigate how the change in peroxo binding mode affects the spectroscopic properties of the metal center.…”

“…68 However, the structure calculated for 1b differs significantly from that proposed by Neese et al for [Fe(EDTA)(η 2 -O 2 )] 3-derived from a detailed spectroscopic analysis. 39 The latter is proposed to have a six-coordinate Fe(III) center with two of four carboxylates of EDTA dissociated from the metal center. The rather long Fe-N amine distance calculated for 1b may indicate a similar tendency toward a six-coordinate structure, but the complete dissociation of the amine ligand may be constrained by the N4Py ligand.…”