An Fe2IVO2 Diamond Core Structure for the Key Intermediate Q of Methane Monooxygenase

A new paradigm for oxygen activation is required for enzymes such as methane monooxygenase (MMO), for which catalysis depends on a nonheme diiron center instead of the more familiar Fe-porphyrin cofactor. On the basis of precedents from synthetic diiron complexes, a high-valent Fe2(μ-O)2 diamond core has been proposed as the key oxidizing species for MMO and other nonheme diiron enzymes such as ribonucleotide reductase and fatty acid desaturase. The presence of a single short Fe-O bond (1.77 angstroms) per Fe atom and an Fe-Fe distance of 2.46 angstroms in MMO reaction intermediate Q, obtained from extended x-ray absorption fine structure and Mössbauer analysis, provides spectroscopic evidence that the diiron center in Q has an Fe2IVO2 diamond core.

[1]  Stephen J. Lippard,et al.  Structure and Mössbauer Spectrum of a (μ-1,2-Peroxo)bis(μ-carboxylato)diiron(III) Model for the Peroxo Intermediate in the Methane Monooxygenase Hydroxylase Reaction Cycle , 1996 .

[2]  J. Penner‐Hahn,et al.  Reduced derivatives of the Mn cluster in the oxygen-evolving complex of photosystem II: An EXAFS study , 1996 .

[3]  B. Fox,et al.  Methane monooxygenase from Methylosinus trichosporium OB3b. Purification and properties of a three-component system with high specific activity from a type II methanotroph. , 1989, The Journal of biological chemistry.

[4]  Stephen J. Lippard,et al.  Kinetic and spectroscopic characterization of intermediates and component interactions in reactions of methane monooxygenase from Methylococcus capsulatus (Bath) , 1995 .

[5]  L. Que,et al.  X-ray Absorption Pre-Edge Studies of High-spin Iron(II) Complexes , 1995 .

[6]  J D Lipscomb,et al.  Large kinetic isotope effects in methane oxidation catalyzed by methane monooxygenase: evidence for C-H bond cleavage in a reaction cycle intermediate. , 1996, Biochemistry.

[7]  K. Hodgson,et al.  Structural characterization of horseradish peroxidase using EXAFS spectroscopy. Evidence for Fe = O ligation in compounds I and II. , 1986, Journal of the American Chemical Society.

[8]  M. V. Rajasekharan,et al.  Modeling the photosynthetic water oxidation center: synthesis, structure, and magnetic properties of [Mn2(.mu.-O)2(.mu.-OAc)(H2O)2(bipy)2](ClO4)3.cntdot.H2O , 1994 .

[9]  J. Widom,et al.  X-ray absorption spectroscopy of iron-tyrosinate proteins , 1984 .

[10]  Thomas G. Spiro,et al.  Characterization of a Diiron(III) Peroxide Intermediate in the Reaction Cycle of Methane Monooxygenase Hydroxylase from Methylococcus capsulatus (Bath) , 1995 .

[11]  J. Dawson,et al.  Probing structure-function relations in heme-containing oxygenases and peroxidases. , 1988, Science.

[12]  K. Hodgson,et al.  X-ray Absorption Spectroscopic Studies of the Diiron Center in Methane Monooxygenase in the Presence of Substrate and the Coupling Protein of the Enzyme System , 1995 .

[13]  H. Dalton,et al.  Resolution of the methane mono-oxygenase of Methylococcus capsulatus (Bath) into three components. Purification and properties of component C, a flavoprotein. , 1978, The Biochemical journal.

[14]  W. Lovenberg.  Iron-sulfur proteins, , 1973 .

[15]  D. Kurtz.  Oxo- and hydroxo-bridged diiron complexes: a chemical perspective on a biological unit , 1990 .

[16]  L. Que,et al.  Exafs studies of binuclear iron proteins hemerythrin and ribonucleotide reductase , 1987 .

[17]  B. Fox,et al.  A Transient Intermediate of the Methane Monooxygenase Catalytic Cycle Containing an FeIVFeIV Cluster , 1993 .

[18]  Stephen J. Lippard,et al.  Crystal structure of a bacterial non-haem iron hydroxylase that catalyses the biological oxidation of methane , 1993, Nature.

[19]  J. Lipscomb,et al.  Transient intermediates of the methane monooxygenase catalytic cycle. , 1993, The Journal of biological chemistry.

[20]  S. Lippard,et al.  Geometry of the soluble methane monooxygenase catalytic diiron center in two oxidation states. , 1995, Chemistry & biology.

[21]  John D. Lipscomb,et al.  Dioxygen Activation by Enzymes Containing Binuclear Non-Heme Iron Clusters. , 1996, Chemical reviews.

[22]  Lawrence Que,et al.  Modeling the Oxygen Activation Chemistry of Methane Monooxygenase and Ribonucleotide Reductase , 1996 .

[23]  J. Lipscomb,et al.  X-ray absorption spectroscopic studies of the methane monooxygenase hydroxylase component from Methylosinus trichosporium OB3b , 1996, JBIC Journal of Biological Inorganic Chemistry.

[24]  Lawrence Que,et al.  Crystal Structure Analysis of a Synthetic Non‐Heme Diiron ? O2 Adduct: Insight into the Mechanism of Oxygen Activation , 1996 .

[25]  Ortiz de Montellano,et al.  Cytochrome P-450: Structure, Mechanism, and Biochemistry , 1986 .

[26]  Interaction of Manganese with Dioxygen and Its Reduced Derivatives , 1994 .

[27]  L. Que,et al.  The First Bis(.mu.-oxo)diiron(III) Complex. Structure and Magnetic Properties of [Fe2(.mu.-O)2(6TLA)2](ClO4)2 , 1995 .

[28]  Jason A. Halfen,et al.  Reversible Cleavage and Formation of the Dioxygen O-O Bond Within a Dicopper Complex , 1996, Science.