Density Functional Study of the Electric Hyperfine Interactions and the Redox-Structural Correlations in the Cofactor of Nitrogenase. Analysis of General Trends in ⁵⁷Fe Isomer Shifts

Abstract

The influence of the interstitial atom, X, discovered in a recent crystallographic study of the MoFe protein of nitrogenase, on the electric hyperfine interactions of (57)Fe has been investigated with density functional theory. A semiempirical theory for the isomer shift, delta, is formulated and applied to the cofactor. The values of delta for the relevant redox states of the cofactor are predicted to be higher in the presence of X than in its absence. The analysis strongly suggests a [Mo(4+)4Fe(2+)3Fe(3+)] oxidation state for the S = 3/2 state M(N). Among C(4-), N(3-), and O(2-), oxide is found to be the least likely candidate for X. The analysis suggests that X should be present in the cofactor states M(OX) and M(R) as well as in the alternative nitrogenases. The calculations of the electric field gradients (EFGs) indicate that the small values for DeltaE(Q) in M(N) result from an extensive cancellation between valence and ligand contributions. X emerges from the analysis of the hyperfine interactions as an ionically bonded species. Its major effect is on the asymmetry parameters for the EFGs at the six equatorial sites, Fe(Eq). A spin-coupling scheme is proposed for the state [Mo(4+)4Fe(2+)3Fe(3+)] that is consistent with the measured (57)Fe A-tensors and DeltaE(Q) values for M(N) and identifies the unique site exhibiting the small A value with the terminal Fe site, Fe(T). The optimized structure of a cofactor model has been calculated for several oxidation states. The study reveals a contraction in the average Fe-Fe distance upon increasing the number of electrons stored in the cluster, in accord with extended X-ray absorption fine structure studies. The reliability of the adopted methodology for predicting redox-structural correlations is tested for cuboidal [4Fe-4S] clusters. The calculations reveal a systematic increase in the S...S sulfide distances, in quantitative agreement with the available data. These trends are rationalized by a simple electrostatic model.

Self‐Assembly of a Tetradecanuclear Iron Nitride Cluster

“…(Et 4 N) 4 3: A pale yellow solution of (Et 4 N) [FeCl 4 ] [24] (0.33 g, 1.01 mmol) in acetonitrile (0.85 mL) was added to an emulsion of (Me 3 Sn) 3 N [25] (0.52 g, 1.02 mmol) in acetonitrile (0.85 mL). The black solution was stirred for 5 min and allowed to stand at room temperature for 11 h. The black mother liquor was decanted from black rectangular plates of other cluster products.…”

“…[18] Initial magnetic measurements suggest an S = 2 ground state for 3. At 295 K, the value of c M T is 5.89 cm 3 [19] usually have triplet ground states.…”

“…[3] Subsequent electron nuclear double resonance (ENDOR) and electron spin echo envelope modulation (ESEEM) evidence has been interpreted as disfavoring nitrogen as atom X. [4] Shortly after the discovery of atom X, it was found that this atom does not exchange under enzyme turnover conditions with dinitrogen, suggesting that it serves a structural and/or electronic role in the cofactor.…”

How many metals does it take to fix N 2 ? A mechanistic overview of biological nitrogen fixation

“…Subsequently, density functional and other studies have been reported (34,(46)(47)(48) incorporating the three alternative light elements, to model the electronic, magnetic, and chemical redox properties of the FeMo cofactor. These studies have found a preference order N Ͼ C Ͼ O; although not proving the element, it is suggestive of nitrogen as the core atom.…”

Bio‐organometallic Approaches to Nitrogen Fixation Chemistry

“…The Hoffman and Münck groups have independently proposed valence assignments for the inorganic portion of the cofactor in its S = 3/2 state using Q-band ENDOR and Mössbauer spectroscopies [22,23]. While a two-electron discrepancy exists in their originally proposed assignments (Mo 4+ /Fe 3+ / 6Fe 2+ versus Mo 4+ /3Fe 3+ /4Fe 2+ ), it is known that during turnover conditions at least three or four Fe protein cycles occur.…”