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Geometric and electronic structures of the His–Fe(IV)=O and His–Fe(IV)–Tyr hemes of MauG

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Abstract

Biosynthesis of the tryptophan tryptophylquinone (TTQ) cofactor activates the enzyme methylamine dehydrogenase. The diheme enzyme MauG catalyzes O-atom insertion and cross-linking of two Trp residues to complete TTQ synthesis. Solution optical and Mössbauer spectroscopic studies have indicated that the reactive form of MauG during turnover is an unusual bisFe(IV) intermediate, which has been formulated as a His-ligated ferryl heme [Fe(IV)=O] (heme A), and an Fe(IV) heme with an atypical His/Tyr ligation (heme B). In this study, Fe K-edge X-ray absorption spectroscopy and extended X-ray absorption fine structure studies have been combined with density functional theory (DFT) and time-dependent DFT methods to solve the geometric and electronic structures of each heme site in the MauG bisFe(IV) redox state. The ferryl heme site (heme A) is compared with the well-characterized compound I intermediate of cytochrome c peroxidase. Heme B is unprecedented in biology, and is shown to have a six-coordinate, S = 1 environment, with a short (1.85-Å) Fe–O(Tyr) bond. Experimentally calibrated DFT calculations are used to reveal a strong covalent interaction between the Fe and the O(Tyr) ligand of heme B in the high-valence form. A large change in the Fe–O(Tyr) bond distance on going from Fe(II) (2.02 Å) to Fe(III) (1.89 Å) to Fe(IV) (1.85 Å) signifies increasing localization of spin density on the tyrosinate ligand upon sequential oxidation of heme B to Fe(IV). As such, O(Tyr) plays an active role in attaining and stabilizing the MauG bisFe(IV) redox state.

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Notes

  1. A first shell with four Fe–N/O components has a slightly better F value, but the 4.5 Fe–N/O fit is more consistent with the crystal structure.

  2. This short distance is consistent with Fe–O distances (1.83–1.94 Å) obtained from a small-molecule database on related species.

  3. Resolution is the separation at which two different metal–ligand paths can be distinguished.

Abbreviations

CCP:

Cytochrome c peroxidase

CCP-I:

Compound I of cytochrome c peroxidase

DFT:

Density functional theory

EXAFS:

Extended X-ray absorption fine structure

HOMO:

Highest occupied molecular orbital

LUMO:

Lowest unoccupied molecular orbital

MADH:

Methylamine dehydrogenase

4MP:

4-Methylphenolate

TD-DFT:

Time-dependent density functional theory

TTQ:

Tryptophan tryptophylquinone

XAS:

X-ray absorption spectroscopy

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Acknowledgments

Portions of this research were performed at the Stanford Synchrotron Radiation Lightsource (SSRL), a Directorate of SLAC National Accelerator Laboratory and an Office of Science User Facility operated for the US Department of Energy Office of Science by Stanford University. The SSRL Structural Molecular Biology Program is supported by the Department of Energy Office of Biological and Environmental Research, and by the National Institutes of Health, the National Institute of General Medical Sciences (including P41GM103393), and the National Center for Research Resources (P41RR001209). C.M.W., V.L.D., and T.L.P were supported by the National Institutes of Health grants GM66569, GM41574, and GM42614, respectively.

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Authors and Affiliations

  1. Department of Biochemistry, Molecular Biology and Biophysics, University of Minnesota, Minneapolis, MN, 55455, USA

    Lyndal M. R. Jensen & Carrie M. Wilmot

  2. Departments of Molecular Biology and Biochemistry, Chemistry, and Pharmaceutical Sciences, University of California, Irvine, CA, 92697, USA

    Yergalem T. Meharenna & Thomas L. Poulos

  3. Burnett School of Biomedical Sciences, College of Medicine, University of Central Florida, Orlando, FL, 32827, USA

    Victor L. Davidson

  4. Stanford Synchrotron Radiation Lightsource, SLAC National Accelerator Laboratory, Menlo Park, CA, 94025, USA

    Britt Hedman & Ritimukta Sarangi

Authors
  1. Lyndal M. R. Jensen
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  2. Yergalem T. Meharenna
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  3. Victor L. Davidson
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Correspondence to Carrie M. Wilmot or Ritimukta Sarangi.

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Jensen, L.M.R., Meharenna, Y.T., Davidson, V.L. et al. Geometric and electronic structures of the His–Fe(IV)=O and His–Fe(IV)–Tyr hemes of MauG. J Biol Inorg Chem 17, 1241–1255 (2012). https://doi.org/10.1007/s00775-012-0939-3

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