A complete biomimetic iron-sulfur cubane redox series

Abstract

Synthetic iron-sulfur cubanes are models for biological cofactors, which are essential to delineate oxidation states in the more complex enzymatic systems. However, a complete series of [Fe₄S₄]ⁿ complexes spanning all redox states accessible by 1-electron transformations of the individual iron atoms (n = 0-4+) has never been prepared, deterring the methodical comparison of structure and spectroscopic signature. Here, we demonstrate that the use of a bulky arylthiolate ligand promoting the encapsulation of alkali-metal cations in the vicinity of the cubane enables the synthesis of such a series. Characterization by EPR, ⁵⁷Fe Mössbauer spectroscopy, UV-visible electronic absorption, variable-temperature X-ray diffraction analysis, and cyclic voltammetry reveals key trends for the geometry of the Fe₄S₄ core as well as for the Mössbauer isomer shift, which both correlate systematically with oxidation state. Furthermore, we confirm the S = 4 electronic ground state of the most reduced member of the series, [Fe₄S₄]⁰, and provide electrochemical evidence that it is accessible within 0.82 V from the [Fe₄S₄]²⁺ state, highlighting its relevance as a mimic of the nitrogenase iron protein cluster.

Keywords: Mössbauer spectroscopy; all-ferrous cubane; electrochemistry; iron-sulfur clusters; nitrogenase.

Fig. 1.

Synthetic strategy used for the isolation and characterization of the redox series K_n[Fe₄S₄(DmpS)₄] (n = 0–4). (A) Stabilization of reduced FeS cubanes in enzymes versus the strategy deployed in this work. (B) Schematic depiction of syntheses, whereby all reactions were carried out in toluene as solvent. Enzymatic systems and their active redox states relevant for the molecular models are indicated alongside.

Fig. 2.

Solid-state molecular structures of 3 (A), 4 (B), 5 (C), 6 (D), and 7 (E) in crystals of K₄[Fe₄S₄(DmpS)₄]⋅2HMDSO, K₃[Fe₄S₄(DmpS)₄]⋅2HMDSO, K₂[Fe₄S₄(DmpS)₄]⋅2HMDSO, K[Fe₄S₄(DmpS)₄]⋅C₇H₈, and [Fe₄S₄(DmpS)₄]⋅HMDSO, respectively. Cocrystallized solvent molecules as well as hydrogen atoms were omitted for clarity. Thermal ellipsoids at the 50% probability level are shown only for the Fe, S, and K atoms. Detailed structural parameters of 3–7 are summarized in SI Appendix, Tables S4–S9 and S11.

Fig. 3.

Electrochemical traverse of the [Fe₄S₄]^{0/1+/2+/3+/4+} redox series. (Top Two Traces) Cyclic voltammograms of 4 recorded in 5 mM THF solution containing 0.3 M K[BArF₂₄] recorded with scan rates of 10 mV s⁻¹ and 1 V s⁻¹, respectively. The first scan is shown. (Bottom Two Traces) Cyclic voltammograms of 6 recorded with a scan rate of 100 mV s⁻¹ in 6 mM THF solution containing 0.3 M K[BArF₂₄] (red lines) and in 7 mM THF solution containing 0.3 M [ⁿBu₄N][PF₆] (gray lines), respectively, as electrolyte. Dotted lines indicate the half-wave potentials and peak potentials of individual redox events. Two subsequent scans are shown in shades of red and gray, respectively. The signal marked by an asterisk only appears after scanning at oxidative potentials and marks the reductive dissociation of DmpS^– ligand from 7, as reported elsewhere (51).

Fig. 4.

⁵⁷Fe Mössbauer, EPR, UV-vis electronic absorption and geometric data for clusters 3–7. (A) Mössbauer spectra (hatched bars) recorded on powder samples at 80 K with a 0.06-T external magnetic field applied parallel to the γ-beam for 4–7 and at zero-field for 3. Simulations are overlaid as gray solid lines and deconvolutions are displayed above. See SI Appendix, Table S2, for the parameter values. Note that for the Mössbauer spectrum of 7, an impurity accounting for 4% of the total Fe content has been subtracted (δ = 0.96 mm s⁻¹, ΔE_Q = 2.09 mm s⁻¹, Γ_fwhm = 0.25 mm s⁻¹). (B) X-band perpendicular mode EPR spectra of 2 mM toluene solutions of 4, recorded at 10 K and 6 (Inset), recorded at 40 K. Data are represented by solid lines and simulations by dotted ones. For details of the fitting parameters, refer to SI Appendix, Figs. S24 and S25. (C, Top) Averaged value of the isomer shift issued from the simulations of the 80-K Mössbauer spectra upon the averaged oxidation state of the iron ions in complexes 3–7. The gray dotted line is a linear fit of the four experimental points. Data recorded on selected biological systems are shown as green dots. (C, Bottom) Variation in the Fe₄ and S₄ core volumes of selected FeS cubane containing structures of biological (FeP, 4Fe-4S Fds, and HiPIP) and synthetic origin. Synthetic models of aromatic thiolate supported cubanes span 8, 11, and 5 examples for [Fe₄S₄(SAr)₄]^1–, [Fe₄S₄(SAr)₄]^2–, and [Fe₄S₄(SAr)₄]^3–, respectively. The data are represented by a gray triangle, dot, and square in the position of the arithmetic mean. Bars indicate the maximum and minimum values reported. Data for the redox series 3–7 are shown by red, blue, yellow, magenta, and cyan diamonds with error bars; refer to SI Appendix, Table S12, for all values and references. (D) UV-vis electronic absorption spectra of 1.1 · 10⁻⁴ M toluene solutions of compounds 3 (red), 4 (blue), 5 (yellow), 6 (magenta), and 7 (cyan). Solid gray lines indicate spectra measured along the stoichiometric redox comproportionation reaction between 3 and 5, which results in the formation of 4.

Fig. 5.

Spectroscopic and structural data for 3. (A) 2.5 K Mössbauer spectrum recorded on a powder sample of 3 using a 7-T external magnetic field applied parallel to the γ-beam (hatched bars). A simulation is overlaid as a gray solid line, and the corresponding list of parameters is given in SI Appendix, Table S3. (B) Low-field region of the parallel-mode EPR spectrum of a 10-mM frozen toluene/cyclohexane (9:1) solution of 3 recorded at 6 K. (C, D) Difference electron density map (–0.74 e/ų (red) to 0.751 e/ų (blue); iso-values in increments of 0.1147 e/ų) of a mean plane through the Fe1-position before (C) and after (D) applying the split model, highlighting the smoothing of the residual electron density upon refining the disorder. (E) Solid-state molecular structure of the Fe₄S₄ unit in 3 at 100 K, containing three symmetry equivalent iron-atoms (Fe1 site with an occupancy of 0.797(8)) and one iron atom of the Fe1A site with an occupancy of 0.203(8). The disorder described by the split model corresponds to a superposition of this locally ordered unit in four different orientations. Distances are given in angstroms.