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

    Authors

    L. M. R. Jensen; Y. T. Meharenna; V. L. Davidson; T. L. Poulos; B. Hedman; C. M. Wilmot;R. Sarangi

    Comments

    Authors: contact us about adding a copy of your work at STARS@ucf.edu

    Abbreviated Journal Title

    J. Biol. Inorg. Chem.

    Keywords

    MauG; Fe K-edge X-ray absorption spectroscopy; High-valence Fe; Density; functional theory; Heme; CYTOCHROME-C PEROXIDASE; TRYPTOPHAN TRYPTOPHYLQUINONE BIOSYNTHESIS; DENSITY-FUNCTIONAL THEORY; ABSORPTION FINE-STRUCTURE; GAUSSIAN-BASIS; SETS; METHYLAMINE DEHYDROGENASE; COMPOUND-I; K-EDGE; OXYGEN ACTIVATION; SPECTROSCOPIC EVIDENCE; Biochemistry & Molecular Biology; Chemistry, Inorganic & Nuclear

    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 Mossbauer 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-) 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 ) to Fe(III) (1.89 ) to Fe(IV) (1.85 ) 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.

    Journal Title

    Journal of Biological Inorganic Chemistry

    Volume

    17

    Issue/Number

    8

    Publication Date

    1-1-2012

    Document Type

    Article

    Language

    English

    First Page

    1241

    Last Page

    1255

    WOS Identifier

    WOS:000311669200010

    ISSN

    0949-8257

    Share

    COinS