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

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 <i>C</i> 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 <i>C</i> 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 <i>C</i> cluster.