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Planar three-coordinate iron sulfide in a synthetic [4Fe-3S] cluster with biomimetic reactivity

Nature Chemistry volume 11, pages 1019–1025 (2019)Cite this article

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Abstract

Iron–sulfur clusters are emerging as reactive sites for the reduction of small-molecule substrates. However, the four-coordinate iron sites of typical iron–sulfur clusters rarely react with substrates, implicating three-coordinate iron. This idea is untested because fully sulfide-coordinated three-coordinate iron is unprecedented. Here we report a new type of [4Fe-3S] cluster that features an iron centre with three bonds to sulfides, and characterize examples of the cluster in three oxidation levels using crystallography, spectroscopy, and ab initio calculations. Although a high-spin electronic configuration is characteristic of other iron–sulfur clusters, the three-coordinate iron centre in these clusters has a surprising low-spin electronic configuration due to the planar geometry and short Fe-S bonds. In a demonstration of biomimetic reactivity, the [4Fe-3S] cluster reduces hydrazine, a natural substrate of nitrogenase. The product is the first example of NH2 bound to an iron–sulfur cluster. Our results demonstrate that three-coordinate iron supported by sulfide donors is a plausible precursor to reactivity in iron–sulfur clusters like the FeMoco of nitrogenase.

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Fig. 1: Preparation and relevance of a series of [4Fe-3S] clusters with trigonal planar iron.
Fig. 2: Structural analogy between [4Fe-3S] and the FeMoco.
Fig. 3: Spectroscopy of three-coordinate [4Fe-3S] clusters and amide-coordinated product 4 gives insight into electronic structures.
Fig. 4: Calculated ligand-field splitting diagram of iron sites in all-ferrous [4Fe-3S][K] (3).
Fig. 5: [4Fe-3S] reactivity with hydrazine and characterization of Fe–NH2 product.

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Data availability

X-ray crystallographic data have been deposited in the Cambridge Crystallographic Data Centre (http://www.ccdc.cam.ac.uk/) with deposition numbers 1879376 ([4Fe-3S][K]), 1879377 ([4Fe-3S][K]2), 1879378 ([4Fe-3S][K]3), 18793769 ([4Fe-3S][Rb]), 1879380 ([4Fe-3S][Rb]2), 1879381 ([4Fe-3S][Cs]), 1879382 ([4Fe-3S][Cs]2) and 1879383 ([4Fe-3S][K]-NH2). Copies of the data can be obtained free of charge via https://www.ccdc.cam.ac.uk/structures/. All other characterization data and experimental methods are provided in this article and its Supplementary Information. Data are also available from the corresponding author on request.

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Acknowledgements

This work was supported by the National Institutes of Health (GM065313 to P.L.H.), the Max Planck Society (E.B., S.D. and F.N.) and IMPRS-RECHARGE (C.V.S.). We thank A. Göbels for measurement of superconducting quantum interference device data and G. Brudvig, G. Banerjee, D. Suess and A. Speelman for help with EPR spectroscopy. We thank C. Cummins and W. Transue for insightful conversations and the gift of Carpino’s hydrazine. Elemental analysis data were measured at the CENTC Elemental Analysis Facility at the University of Rochester, funded by the NSF (CHE-0650456), and we thank W. Brennessel for collecting these data. XAS spectra were measured at SSRL 9-3 and ESRF ID-26 and we thank M. Latimer and B. Detlefs for their assistance during measurements. Use of SSRL is supported by the DOE, BES (DE-AC02-76SF00515). The SSRL SMB programme is supported by DOE, BER and NIH (including P41GM103393).

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Authors and Affiliations

  1. Department of Chemistry, Yale University, New Haven, CT, USA

    Daniel E. DeRosha, Brandon Q. Mercado & Patrick L. Holland

  2. Max Planck Institute for Coal Research, Mülheim an der Ruhr, Germany

    Vijay G. Chilkuri & Frank Neese

  3. Max Planck Institute for Chemical Energy Conversion, Mülheim an der Ruhr, Germany

    Casey Van Stappen, Eckhard Bill & Serena DeBeer

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Contributions

D.E.D. performed the synthetic experiments, and collected and analysed spectroscopic data. B.Q.M. and D.E.D. collected and interpreted crystallographic data. C.V.S. and S.D. collected and interpreted the X-ray absorption data. V.G.C. and F.N. performed and interpreted the computational and theoretical aspects. E.B. performed superconducting quantum interference device and magnetic Mössbauer measurements and analyses. P.L.H. supervised the research and D.E.D. and P.L.H. wrote the manuscript.

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Correspondence to Patrick L. Holland.

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DeRosha, D.E., Chilkuri, V.G., Van Stappen, C. et al. Planar three-coordinate iron sulfide in a synthetic [4Fe-3S] cluster with biomimetic reactivity. Nat. Chem. 11, 1019–1025 (2019). https://doi.org/10.1038/s41557-019-0341-7

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