Inserting Three-Coordinate Nickel into [4Fe-4S] Clusters

Abstract

Metalloenzymes can efficiently achieve the multielectron interconversion of carbon dioxide and carbon monoxide under mild conditions. Anaerobic carbon monoxide dehydrogenase (CODH) performs these reactions at the C cluster, a unique nickel-iron-sulfide cluster that features an apparent three-coordinate nickel site. How nature assembles the [NiFe₃S₄]-Fe_u cluster is not well understood. We use synthetic clusters to demonstrate that electron transfer can drive insertion of a Ni⁰ precursor into an [Fe₄S₄]³⁺ cluster to assemble higher nuclearity nickel-iron-sulfide clusters with the same complement of metal ions as the C cluster. Initial electron transfer results in a [1Ni-4Fe-4S] cluster in which a Ni¹⁺ ion sits outside of the cluster. Modifying the Ni⁰ precursor results in the insertion of two nickel atoms into the cluster, concomitant with ejection of an iron to yield an unprecedented [2Ni-3Fe-4S] cluster possessing four three-coordinate metal sites. Both clusters are characterized using magnetometry, electron paramagnetic resonance (EPR), Mössbauer, and X-ray absorption spectroscopy and supported by DFT computations that are consistent with both clusters having nickel in the +1 oxidation state. These results demonstrate that Ni¹⁺ is a viable oxidation state within iron-sulfur clusters and that redox-driven transformations can give rise to higher nuclearity clusters of relevance to the CODH C cluster.

Figure 1

(a) Two catalytically relevant oxidation states of the C cluster in CODH that feature a three-coordinate nickel site. (b) Previously reported synthetic iron–sulfur clusters that contain four-coordinate nickel sites. (c) The first example of a three-coordinate nickel site in a synthetic iron–sulfur cluster. Tp* = tris(3,5-dimethyl-1-pyrazolyl)borate.

Figure 2

(a) Proposed biosynthesis of the C cluster. (b) Synthetic route to the NiFe₄S₄ cluster. (c) Molecular structure of NiFe₄S₄ as determined by single-crystal X-ray diffraction presented from two view perspectives. Orange, yellow, green, blue, pink and gray represent iron, sulfur, nickel, nitrogen, silicon, and carbon atoms, respectively. Anisotropic displacement ellipsoids depicted at 50% probability. The outer sphere cation, hydrogen atoms, and solvent molecules are omitted for clarity, and the right view additionally omits most silicon and some carbon substituents.

Figure 3

(a) Synthetic route to the Ni₂Fe₃S₄ cluster. (b) Molecular structures of Ni₂Fe₃S₄ as determined by single-crystal X-ray diffraction. Orange, yellow, green, blue, gray, and pink represent iron, sulfur, nickel, nitrogen, carbon, and sodium atoms, respectively. Anisotropic displacement ellipsoids depicted at 50% probability. The 2,6-diisopropylphenyl and N(SiMe₃)₂ moieties are represented as spheres of arbitrary radius, and hydrogen atoms and solvent molecules are omitted for clarity.

Figure 4

(a) Stacked Mössbauer spectra of NiFe₄S₄ and Ni₂Fe₃S₄ at 80 K. NiFe₄S₄: δ = 0.46 mm s^–1 (δ_DFT = 0.44 mm s^–1), |ΔE_Q| = 1.03 mm s^–1, Γ = 0.56 mm s^–1. Ni₂Fe₃S₄, site 1 (green, 67%): δ₁ = 0.49 mm s^–1 (δ_1,DFT = 0.39 mm s^–1), |ΔE_Q|₁ = 0.75 mm s^–1, Γ₁ = 0.36 mm s^–1; site 2 (blue, 33%): δ₂ = 0.34 mm s^–1 (δ_2,DFT = 0.35 mm s^–1), |ΔE_Q|₂ = 0.83 mm s^–1, Γ₂ = 0.28 mm s^–1. (b) Experimental δ values for NiFe₄S₄ and Ni₂Fe₃S₄ relative to structurally analogous amide-supported Fe₄S₄ clusters and to thiolate-supported linear chain Fe₃S₄ clusters from the literature.^,

Figure 5

(a) Overlay of the dc magnetic susceptibility data for NiFe₄S₄ (blue) and Ni₂Fe₃S₄ (red) collected under an applied magnetic field of 0.1 T. (b) EPR spectrum of a frozen solution of NiFe₄S₄ in toluene (2 mM) collected at 9.38 GHz and 5 K. (c) EPR spectrum of a solid sample of Ni₂Fe₃S₄ collected at 9.38 GHz and 10 K.

Figure 6

(a) X-ray absorption spectra at the iron and nickel K-edges, with derivative spectra below. In the Fe XAS of NiFe₄S₄ and Ni₂Fe₃S₄, the pre-edges are found at 7112.2 and 7112.4 eV, while the first-derivative maxima are found at 7116.9 and 7115.6 eV, respectively. (b) Spin coupling schemes for NiFe₄S₄ (top) and Ni₂Fe₃S₄ (bottom); arrows represent dominantly antiferromagnetic exchange interactions.

Figure 7

Redox transformation of the C cluster, as demonstrated by X-ray crystallographic studies on D. vulgaris CO dehydrogenase. Reprinted with permission from ref (23). Copyright 2018 eLife; used under a CC-BY license.