An abiotic analogue of the diiron(iv)oxo “diamond core” of soluble methane monooxygenase generated by direct activation of O2 in aqueous Fe(ii)/EDTA solutions: thermodynamics and electronic structure

Abstract

We study the generation of a dinuclear Fe(IV)oxo species, [EDTAH·FeO·OFe·EDTAH](2-), in aqueous solution at room temperature using Density Functional Theory (DFT) and Ab Initio Molecular Dynamics (AIMD). This species has been postulated as an intermediate in the multi-step mechanism of autoxidation of Fe(II) to Fe(III) in the presence of atmospheric O(2) and EDTA ligand in water. We examine the formation of [EDTAH·FeO·OFe·EDTAH](2-) by direct cleavage of O(2), and the effects of solvation on the spin state and O-O cleavage barrier. We also study the reactivity of the resulting dinuclear Fe(IV)oxo system in CH(4) hydroxylation, and its tendency to decompose to mononuclear Fe(IV)oxo species. The presence of the solvent is shown to play a crucial role, determining important changes in all these processes compared to the gas phase. We show that, in water solution, [EDTAH·FeO·OFe·EDTAH](2-) (as well as its precursor [EDTAH·Fe·O(2)·Fe·EDTAH](2-)) exists as stable species in a S = 4 ground spin state when hydrogen-bonded to a single water molecule. Its structure comprises two facing Fe(IV)oxo groups, in an arrangement similar to the one evinced for the active centre of intermediate Q of soluble Methane Monooxygenase (sMMO). The inclusion of the water molecule in the complex decreases the overall symmetry of the system, and brings about important changes in the energy and spatial distribution of orbitals of the Fe(IV)oxo groups relative to the gas phase. In particular, the virtual 3σ* orbital of one of the Fe(IV)oxo groups experiences much reduced repulsive orbital interactions from ligand orbitals, and its consequent stabilisation dramatically enhances the electrophilic character of the complex, compared to the symmetrical non-hydrated species, and its ability to act as an acceptor of a H atom from the CH(4) substrate. The computed free energy barrier for H abstraction is 28.2 kJ mol(-1) (at the BLYP level of DFT), considerably below the gas phase value for monomeric [FeO·EDTAH](-), and much below the solution value for the prototype hydrated ferryl ion [FeO(H(2)O)(5)](2+).

Applications of density functional theory to iron-containing molecules of bioinorganic interest

“…Theoretical studies of such biomimetic models may not only identify the key elements that determine their chemical reactivities, but may also provide insight into intermediates and reactivities of parent enzymes (Shaik et al, 2007a; de Visser et al, 2013). To date, DFT calculations have been applied extensively to various types of non-heme iron species (Scheme 1) (Bassan et al, 2002, 2005a,b; Roelfes et al, 2003; Decker and Solomon, 2005; Kumar et al, 2005; Quinonero et al, 2005; Berry et al, 2006; Bernasconi et al, 2007, 2011; de Visser, 2006, 2010; Hirao et al, 2006a, 2008a,b, 2011; Rohde et al, 2006; Decker et al, 2007; de Visser et al, 2007, 2011; Johansson et al, 2007; Noack and Siegbahn, 2007; Sastri et al, 2007; Sicking et al, 2007; Bernasconi and Baerends, 2008, 2013; Comba et al, 2008; Dhuri et al, 2008; Fiedler and Que, 2009; Klinker et al, 2009; Wang et al, 2009a, 2013b; Cho et al, 2010, 2012a, 2013; Geng et al, 2010; Chen et al, 2011; Chung et al, 2011b; Seo et al, 2011; Shaik et al, 2011; Vardhaman et al, 2011; Wong et al, 2011; Ye and Neese, 2011; Gonzalez-Ovalle et al, 2012; Gopakumar et al, 2012; Latifi et al, 2012; Mas-Ballesté et al, 2012; McDonald et al, 2012; Van Heuvelen et al, 2012; Ansari et al, 2013; Kim et al, 2013; Lee et al, 2013; Sahu et al, 2013; Tang et al, 2013; Ye et al, 2013; Hong et al, 2014; Sun et al, 2014). The intriguing reactivity patterns of these complexes are the result of active involvement of electrons in d-type MOs, which gives rise to multi-state scenarios (Shaik et al, 1998; Schröder et al, 2000; Schwarz, 2011).…”

Density-functional theory models of Fe(iv)O reactivity in metal–organic frameworks: self-interaction error, spin delocalisation and the role of hybrid exchange

“…Therefore, the goal of this work is to address these limitations by examining the influence of exchange-correlation functional choice specifically on the predicted reactivity of MOF-74 supported Fe(IV)O. We show that conventional generalisedgradient approximations (GGAs), like PBE 24 and BLYP, 25,26 which typically provide an accurate description both of the structural/ vibrational properties of MOFs 27 and of Fe(IV)O catalysed hydroxylation reactions in the gas phase and in aqueous solution 28,29 yield a qualitatively incorrect description of the H-abstraction reaction profile from methane in the solid state. We attribute this failure to the self-interaction error (SIE) affecting these functionals, which brings about a spurious mixing between reactant (CH 4 ) orbitals and extended MOF-74 states.…”

Electronic structure and reactivity of Fe(iv)oxo species in metal–organic frameworks

“…By contrast, single-state (quintet) reactivity has been observed in Fe(IV)O complexes in the gas phase and in water solution. 31 A more detailed analysis of two-(or multi-) state reactivity for Fe(IV)O/ MOF-74 (which can affect, inter alia, the mechanism and rate constant of the hydroxylation reaction 58 ) will be presented elsewhere. Future work will also be devoted to studying the effect of the exchange-correlation approximation on the electronic structure and on the reactivity of Fe(IV)O/MOF-74 as well as to compute free-energies of reaction at room temperature.…”

“…The ability of Fe(IV)O complexes to oxidise methane in aqueous solution has also been examined, and the presence of the solvent has been shown to play a crucial role in favouring the reaction. [31][32][33] In the presence of suitable coordination environments for hydrogen abstraction reactions carried out in water solution at room temperature, freeenergy barriers as low as ca. 30 kJ mol À1 have been predicted on the basis of DFT calculations, to be compared to an estimate of ca.…”

“…As mentioned above, it has been shown that the catalytic activity of Fe(IV)O species is strongly influenced by the coordination environment of the Fe ion. 19,21,31 In particular, it has been demonstrated that an oxygen-rich Fe coordination environment stabilises the most reactive (quintet) spin state of the Fe(IV)O moiety and decreases the energy of its lowest virtual orbital (3s*), which is responsible for the electrophilic character, and therefore for the catalytic activity, of Fe(IV)O in hydrocarbon oxidation. 21 The structure of MOF-74 offers, in principle, an ideal coordination framework capable of stabilising highly reactive Fe(IV)O species.…”