Gauging Iron-Sulfur Cubane Reactivity from Covalency: Trends with Oxidation State

Abstract

We investigated room-temperature metal and ligand K-edge X-ray absorption (XAS) spectra of a complete redox series of cubane-type iron-sulfur clusters. The Fe K-edge position provides a qualitative but convenient alternative to the traditional spectroscopic descriptors used to identify oxidation states in these systems, which we demonstrate by providing a calibration curve based on two analytic methods. Furthermore, high energy resolution fluorescence detected XAS (HERFD-XAS) at the S K-edge was used to measure Fe-S bond covalencies and record their variation with the average valence of the Fe atoms. While the Fe-S(thiolate) covalency evolves linearly, gaining 11 ± 0.4% per bond and hole, the Fe-S(μ³) covalency evolves asystematically, reflecting changes in the magnetic exchange mechanism. A strong discontinuity manifested for superoxidation to the all-ferric state, distinguishing its electronic structure and its potential (bio)chemical role from those of its redox congeners. We highlight the functional implications of these trends for the reactivity of iron-sulfur cubanes.

Scheme 1. Molecular Structure of the [Fe₄S₄(^CysS)₄]^n– Cofactor Model, K_n[Fe₄S₄(DmpS)₄] (Where n = 0-4)

R refers to 2,6-dimesitylphenyl (Dmp).

Figure 1

(A) Normalized Fe K-edge XAS spectra of the K_n[Fe₄S₄(DmpS)₄] (n = 0–4) powdered samples measured at room temperature. The inset shows the correlation between the average Fe oxidation state (average valence) and the energy of the inflection point (E₀); a linear fit of these data is presented as a dotted gray line, indicating an increase in E₀ of 0.57 ± 0.03 eV per 1-electron oxidation. (B) Unfiltered EXAFS spectra of the K_n[Fe₄S₄(DmpS)₄] (n = 0–4; gray dots) in k-space, and the corresponding fits (colored lines). The range over which the fit was carried out is shaded in gray. (C) FT-EXAFS spectra (k²-weighted) of K_n[Fe₄S₄(DmpS)₄] (n = 0–4).

Figure 2

Normalized S K-edge HERFD-XAS spectra of K_n[Fe₄S₄(DmpS)₄] (n = 0–4) recorded on powdered samples at room temperature in vacuo.

Figure 3

(A) Variation of covalency, α², and its individual contributions with the average valence of the Fe-atom. While the total α² is shown as colored diamonds ([Fe₄S₄]⁴⁺: cyan, [Fe₄S₄]³⁺: magenta, [Fe₄S₄]²⁺: yellow, [Fe₄S₄]¹⁺: blue, [Fe₄S₄]⁰: red), contributions arising from sulfide- and thiolate-bonding are presented as dot and triangle shaped markers, respectively. Dotted gray lines are intended to guide the eye. Approximate error bars are shown in gray color; for details on the error estimation, refer to the Supporting Information. (B) Net change in the covalency upon redox transformations of the [Fe₄S₄]²⁺ cubane per Fe-atom: superreduction to [Fe₄S₄]⁰ (red), ferredoxin (Fd) type reduction to [Fe₄S₄]¹⁺ (blue), high-potential iron–sulfur protein (HiPIP) type oxidation to [Fe₄S₄]³⁺ (magenta) and superoxidation to [Fe₄S₄]⁴⁺ (cyan). The covalency change relative to the resting oxidation state ([Fe₄S₄]²⁺ in percent (%) is indicated on the individual bars: white font for covalency decrease, black font for covalency increase.

Figure 4

H-bonds (dashed green; values in Å; given as distance from the H-bond donor to the acceptor atom) detected in the second sphere of the FeS cofactor in the crystal structure of thermochromatium tepidum HiPIP (PDB code 5WQR(49)) in the reduced ([Fe₄S₄]²⁺) oxidation state. H-bonds were calculated according to the criteria described by Mills and Dean, relaxing the angle and distance tolerances by 20° and 0.4 Å, respectively. This figure was generated using the ChimeraX program suite.^,