JBIC Journal of Biological Inorganic Chemistry

, Volume 24, Issue 6, pp 793–807 | Cite as

Radical S-adenosylmethionine maquette chemistry: Cx3Cx2C peptide coordinated redox active [4Fe–4S] clusters

  • Amanda Galambas
  • Jacquelyn Miller
  • Morgan Jones
  • Elizabeth McDaniel
  • Molly Lukes
  • Hope Watts
  • Valérie Copié
  • Joan B. Broderick
  • Robert K. SzilagyiEmail author
  • Eric M. ShepardEmail author
Original Paper
Part of the following topical collections:
  1. Joan Broderick: Papers in Celebration of Her 2019 ACS Alfred Bader Award in Bioinorganic or Bioorganic Chemistry


The synthesis and characterization of short peptide-based maquettes of metalloprotein active sites facilitate an inquiry into their structure/function relationships and evolution. The [4Fe–4S]-maquettes of bacterial ferredoxin metalloproteins (Fd) have been used in the past to engineer redox active centers into artificial metalloenzymes. The novelty of our study is the application of maquettes to the superfamily of [4Fe–4S] cluster and S-adenosylmethionine-dependent radical metalloenzymes (radical SAM). The radical SAM superfamily enzymes contain site-differentiated, redox active [4Fe–4S] clusters coordinated to Cx3Cx2C or related motifs, which is in contrast to the Cx2Cx2C motif found in bacterial ferredoxins (Fd). Under an optimized set of experimental conditions, a high degree of reconstitution (80–100%) was achieved for both radical SAM- and Fd-maquettes. Negligible chemical speciation was observed for all sequences, with predominantly [4Fe–4S]2+ for the ‘as-reconstituted’ state. However, the reduction of [4Fe–4S]2+-maquettes provides low conversion (7–17%) to the paramagnetic [4Fe–4S]+ state, independent of either the spacing of the cysteine residues (Cx3Cx2C vs. Cx2Cx2C), the nature of intervening amino acids, or the length of the cluster binding motif. In the absence of the stabilizing protein environment, the reduction process is proposed to proceed via [4Fe–4S]2+ cluster disassembly and reassembly in a more reduced state. UV–Vis and EPR spectroscopic techniques are employed as analytical tools to quantitate the as-reconstituted (or oxidized) and one-electron reduced states of the [4Fe–4S] clusters, respectively. We demonstrate that short Fd and radical SAM derived 7- to 9-mer peptides containing appropriate cysteine motifs function equally well in coordinating redox active [4Fe–4S] clusters.

Graphic abstract


Iron sulfur clusters [4Fe–4S]-maquettes Ferredoxin Radical S-adenosylmethionine UV–Vis spectroscopy Electron paramagnetic resonance spectroscopy Protoenzymes Cysteine motifs 



The authors acknowledge the financial support from NSF Chemistry of Life Processes program Grant #1609557. The work on PFL-AE was supported by the National Institutes of Health GM 54608 (to J.B.B.).

Supplementary material

775_2019_1708_MOESM1_ESM.pdf (1.9 mb)
Details of UV–Vis spectral simulations, UV–Vis spectra of reconstitution experiments in the absence of peptide, EPR properties of [4Fe–4S]+-maquettes, reducing agent dependent EPR spectra, spectroscopic characterization of FdM control maquettes, time-elapsed UV–Vis spectra of as-reconstituted ferredoxin maquettes, redox cycling of radical SAM maquettes, wide-field EPR spectra, and EPR spectral simulations are provided as ESM


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© Society for Biological Inorganic Chemistry (SBIC) 2019

Authors and Affiliations

  1. 1.Department of Chemistry and BiochemistryMontana State UniversityBozemanUSA

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