Biological Methane Oxidation: Regulation, Biochemistry, and Active Site Structure of Particulate Methane Monooxygenase

Particulate methane monooxygenase (pMMO) is a threesubunit integral membrane enzyme that catalyzes the oxidation of methane to methanol. Although pMMO is the predominant methane oxidation catalyst in nature, it has proved difficult to isolate, and most questions regarding its molecular structure, active site composition, chemical mechanism, and genetic regulation remain unanswered. Copper ions are believed to play a key role in both pMMO regulation and catalysis, and there is some evidence that the enzyme contains iron as well. A number of research groups have solubilized and purified or partially purified pMMO. These preparations have been characterized by biochemical and biophysical methods. In addition, aspects of methane monooxygenase gene regulation and copper accumulation in methanotrophs have been studied. This review summarizes for the first time the often controversial pMMO literature, focusing on recent progress and highlighting unresolved issues.

[1]  M. Lidstrom,et al.  Role of multiple gene copies in particulate methane monooxygenase activity in the methane-oxidizing bacterium Methylococcus capsulatus Bath. , 1999, Microbiology.

[2]  W. Liesack,et al.  Isolation of acidophilic methane-oxidizing bacteria from northern peat wetlands. , 1998, Science.

[3]  S. Lippard,et al.  Studies of the Soluble Methane Monooxygenase Protein System: Structure, Component Interactions, and Hydroxylation Mechanism , 1995 .

[4]  Sunney I. Chan,et al.  The Stereospecific Hydroxylation of [2,2-2H2]Butane and Chiral Dideuteriobutanes by the Particulate Methane Monooxygenase from Methylococcus capsulatus (Bath)* , 2003, Journal of Biological Chemistry.

[5]  D. Janssen,et al.  Formation and detoxification of reactive intermediates in the metabolism of chlorinated ethenes. , 2001, Journal of biotechnology.

[6]  C. Brantner,et al.  Intracellular localization of the particulate methane monooxygenase and methanol dehydrogenase in Methylomicrobium album BG8 , 2002, Archives of Microbiology.

[7]  J. Murrell,et al.  Regulation of expression of methane monooxygenases by copper ions. , 2000, Trends in microbiology.

[8]  B. E. Jones,et al.  An obligate methylotrophic, methane-oxidizing Methylomicrobium species from a highly alkaline environment , 2000, Extremophiles.

[9]  I. Okura,et al.  The role of copper in particulate methane monooxygenase from Methylosinus trichosporium OB3b , 1999 .

[10]  Michigan.,et al.  Toxicological profile for dichloropropenes , 2008 .

[11]  J. Bowman,et al.  Revised Taxonomy of the Methanotrophs: Description of Methylobacter gen. nov., Emendation of Methylococcus, Validation of Methylosinus and Methylocystis Species, and a Proposal that the Family Methylococcaceae Includes Only the Group I Methanotrophs , 1993 .

[12]  M. Lidstrom,et al.  Cloning and characterization of corA, a gene encoding a copper-repressible polypeptide in the type I methanotroph, Methylomicrobium albus BG8. , 1997, FEMS Microbiology Letters.

[13]  M. Collins,et al.  Concentration of Cu, EPR-detectable Cu, and formation of cupric-ferrocyanide in membranes with pMMO. , 1998, Journal of inorganic biochemistry.

[14]  H. Schägger,et al.  Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. , 1991, Analytical biochemistry.

[15]  J. Semrau,et al.  Methane and Trichloroethylene Degradation byMethylosinus trichosporium OB3b Expressing Particulate Methane Monooxygenase , 1998, Applied and Environmental Microbiology.

[16]  D. Graham,et al.  Isolation of Copper Biochelates fromMethylosinus trichosporium OB3b and Soluble Methane Monooxygenase Mutants , 1998, Applied and Environmental Microbiology.

[17]  R. Whittenbury,et al.  Enrichment, isolation and some properties of methane-utilizing bacteria. , 1970, Journal of general microbiology.

[18]  M. Lidstrom,et al.  The role of copper in the pMMO of Methylococcus capsulatus bath: a structural vs. catalytic function. , 1995, Journal of inorganic biochemistry.

[19]  P. Singleton,et al.  Detergent solubilization of membrane-bound methane monooxygenase requires plastoquinol analogs as electron donors. , 1995, Archives of biochemistry and biophysics.

[20]  H. Michel,et al.  Crystallization of membrane proteins. , 1983, Current opinion in structural biology.

[21]  A. K. Shiemke,et al.  Evidence that copper is a required cofactor for the membrane-bound form of methane monooxygenase , 1996 .

[22]  M. Lidstrom,et al.  The nature of the copper ions in the membranes containing the particulate methane monooxygenase from Methylococcus capsulatus (Bath). , 1994, The Journal of biological chemistry.

[23]  R. Periana,et al.  A Mercury-Catalyzed, High-Yield System for the Oxidation of Methane to Methanol , 1993, Science.

[24]  Lewis Semprini,et al.  Diversity in Butane Monooxygenases among Butane-Grown Bacteria , 1999, Applied and Environmental Microbiology.

[25]  Thomas E Hanson,et al.  Methanotrophic bacteria. , 1996, Microbiological reviews.

[26]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[27]  A Costello,et al.  Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. , 1995, FEMS microbiology letters.

[28]  Maarten Merkx,et al.  Dioxygen Activation and Methane Hydroxylation by Soluble Methane Monooxygenase: A Tale of Two Irons and Three Proteins. , 2001, Angewandte Chemie.

[29]  M. Kalyuzhnaya,et al.  Isolation and Characterization of Halotolerant Alkaliphilic Methanotrophic Bacteria from Tuva Soda Lakes , 1997, Current Microbiology.

[30]  S. Elliott,et al.  Pulsed EPR Studies of Particulate Methane Monooxygenase from Methylococcus Capsulatus (Bath): Evidence for Histidine Ligation , 1998 .

[31]  J. Murrell,et al.  Molecular Analysis of the pmo (Particulate Methane Monooxygenase) Operons from Two Type II Methanotrophs , 2000, Applied and Environmental Microbiology.

[32]  Richard S. J. Tol,et al.  Methane Emission Reduction: An Application of FUND , 2003 .

[33]  P. Epstein.  Is global warming harmful to health? , 2000, Scientific American.

[34]  H. Dalton,et al.  A low-molecular-mass protein from Methylococcus capsulatus (Bath) is responsible for the regulation of formaldehyde dehydrogenase activity in vitro. , 1999, Microbiology.

[35]  S. Elliott,et al.  Regio- and Stereoselectivity of Particulate Methane Monooxygenase from Methylococcus capsulatus (Bath) , 1997 .

[36]  R. Whittenbury,et al.  The Methylotrophic Bacteria , 1981 .

[37]  A. Rosenzweig,et al.  Purified particulate methane monooxygenase from Methylococcus capsulatus (Bath) is a dimer with both mononuclear copper and a copper-containing cluster , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[38]  M. Lidstrom,et al.  Study of copper accumulation by the type I methanotroph Methylomicrobium albus BG8 , 1996 .

[39]  M. Merkx,et al.  Why OrfY? , 2002, The Journal of Biological Chemistry.

[40]  A Elofsson,et al.  Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. , 1997, Protein engineering.

[41]  N. Priestley,et al.  Tritiated Chiral Alkanes as Substrates for Soluble Methane Monooxygenase from Methylococcus capsulatus (Bath): Probes for the Mechanism of Hydroxylation , 1997 .

[42]  M. Lidstrom,et al.  Particulate methane monooxygenase genes in methanotrophs , 1995, Journal of bacteriology.

[43]  J. V. Van Beeumen,et al.  Purification, characterization, and preliminary crystallographic study of copper-containing nitrous oxide reductase from Pseudomonas nautica 617. , 2000, Biochemistry.

[44]  G. Salmond,et al.  The methane monooxygenase gene cluster of Methylococcus capsulatus (Bath). , 1990, Gene.

[45]  A. Chrambach,et al.  Solubilization of functional membrane proteins. , 1984, Methods in enzymology.

[46]  I. Okura,et al.  Electron Spin-Echo Envelope Modulation Studies on Copper Site of Particulate Methane Monooxygenase from Methylosinus trichosporium OB3b. , 1999 .

[47]  J. Murrell,et al.  rpoN, mmoR and mmoG, genes involved in regulating the expression of soluble methane monooxygenase in Methylosinus trichosporium OB3b. , 2003, Microbiology.

[48]  M. Lidstrom,et al.  Trichloroethylene oxidation by the membrane-associated methane monooxygenase in type I, type II and type X methanotrophs , 2004, Biodegradation.

[49]  J. Hettiaratchi,et al.  Methane Oxidation in Three Alberta Soils: Influence of Soil Parameters and Methane Flux Rates , 2001, Environmental technology.

[50]  C Cambillau,et al.  Revisiting the Catalytic CuZ Cluster of Nitrous Oxide (N2O) Reductase , 2000, The Journal of Biological Chemistry.

[51]  T. Kamachi,et al.  Improvement of the purification method for retaining the activity of the particulate methane monooxygenase from Methylosinus trichosporium OB3b , 2002, Biotechnology Letters.

[52]  S. Elliott,et al.  The Particulate Methane Monooxygenase from Methylococcus capsulatus (Bath) Is a Novel Copper-containing Three-subunit Enzyme , 1998, The Journal of Biological Chemistry.

[53]  Li-Min Zhu,et al.  Particulate methane monooxygenase from Methylosinus trichosporium is a copper-containing enzyme. , 2002, Biochemical and biophysical research communications.

[54]  S. Eaton,et al.  Comparison of EPR-visible Cu(2+) sites in pMMO from Methylococcus capsulatus (Bath) and Methylomicrobium album BG8. , 2000, Biophysical journal.

[55]  I. Okura,et al.  Properties of the membranes containing the particulate methane monooxygenase from Methylosinus trichosporium OB3b , 1998, Biometals.

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

[57]  N. Priestley,et al.  A Concerted Mechanism for Ethane Hydroxylation by the Particulate Methane Monooxygenase from Methylococcus capsulatus (Bath) , 1996 .

[58]  K. Henriksen,et al.  Characterization of Methanotrophic Bacterial Populations in Soils Showing Atmospheric Methane Uptake , 1999, Applied and Environmental Microbiology.

[59]  S. Lippard,et al.  Substrate binding and C-H bond activation in the soluble methane monooxygenase hydroxylase , 1998, JBIC Journal of Biological Inorganic Chemistry.

[60]  K. Hodgson,et al.  X-ray absorption edge determination of the oxidation state and coordination number of copper: application to the type 3 site in Rhus vernicifera laccase and its reaction with oxygen , 1987 .

[61]  D. Scott,et al.  Substrate Specificities of the Soluble and Particulate Methane Mono-oxygenases of Methylosinus trichosporium OB3b , 1984 .

[62]  D. Harrison,et al.  Purification and properties of the methane mono-oxygenase enzyme system from Methylosinus trichosporium OB3b. , 1977, The Biochemical journal.

[63]  S. Elliott,et al.  X-ray Absorption and EPR Studies on the Copper Ions Associated with the Particulate Methane Monooxygenase from Methylococcus capsulatus (Bath). Cu(I) Ions and Their Implications , 1996 .

[64]  M. Collins,et al.  Low-Frequency EPR of the Copper in Particulate Methane Monooxygenase from Methylomicrobium albus BG8 , 1997 .

[65]  M Wilmanns,et al.  Crystal structure of the membrane-exposed domain from a respiratory quinol oxidase complex with an engineered dinuclear copper center. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[66]  D. Arp,et al.  Isolation and characterization of alkane-utilizing Nocardioides sp. strain CF8. , 2000, FEMS microbiology letters.

[67]  R. Gvozdev,et al.  A continuous-wave electron-nuclear double resonance (X-band) study of the Cu2+ sites of particulate methane mono-oxygenase of Methylococcus capsulatus (strain M) in membrane and pure dopamine beta-mono-oxygenase of the adrenal medulla. , 2002, Biochemical Journal.

[68]  J. Sullivan,et al.  Methanotrophs, Methylosinus trichosporium OB3b, sMMO, and their application to bioremediation. , 1998, Critical reviews in microbiology.

[69]  J. Bowman,et al.  Methylosphaera hansonii gen. nov., sp. nov., a psychrophilic, group I methanotroph from Antarctic marine-salinity, meromictic lakes. , 1997, Microbiology.

[70]  H. Dalton,et al.  The effect of copper ions on membrane content and methane monooxygenase activity in methanol-grown cells of Methylococcus capsulatus (Bath) , 1985 .

[71]  R. Friesner,et al.  Mechanistic studies on the hydroxylation of methane by methane monooxygenase. , 2003, Chemical reviews.

[72]  Yane-Shih Wang,et al.  Determination of the Carbon Kinetic Isotope Effects on Propane Hydroxylation Mediated by the Methane Monooxygenases from Methylococcus capsulatus (Bath) by Using Stable Carbon Isotopic Analysis , 2002, Chembiochem : a European journal of chemical biology.

[73]  J. Møller,et al.  Interaction of membrane proteins and lipids with solubilizing detergents. , 2000, Biochimica et biophysica acta.

[74]  J. Lipscomb.  Biochemistry of the soluble methane monooxygenase. , 1994, Annual review of microbiology.

[75]  G. E. Speitel,et al.  Methylosinus trichosporium OB3b Mutants Having Constitutive Expression of Soluble Methane Monooxygenase in the Presence of High Levels of Copper , 1992, Applied and environmental microbiology.

[76]  N. Priestley,et al.  Cryptic stereospecificity of methane monooxygenase , 1992 .

[77]  L. Huan,et al.  Novel method for evaluation of the oligomeric structure of membrane proteins. , 1999, The Biochemical journal.

[78]  I. Okura,et al.  Role of iron and copper in particulate methane monooxygenase of Methylosinus trichosporium OB3b , 2000 .

[79]  P. Wood,et al.  Suicidal inactivation and labelling of ammonia mono-oxygenase by acetylene. , 1985, The Biochemical journal.

[80]  H. Degn,et al.  Regulation of bacterial methane oxidation: transcription of the soluble methane mono-oxygenase operon of Methylococcus capsulatus (Bath) is repressed by copper ions. , 1996, Microbiology.

[81]  H. Dalton,et al.  The membrane-associated form of methane mono-oxygenase from Methylococcus capsulatus (Bath) is a copper/iron protein. , 2003, The Biochemical journal.

[82]  I Mangelsdorf,et al.  Vinyl chloride: still a cause for concern. , 2000, Environmental health perspectives.

[83]  C. Anthony,et al.  The Biochemistry of Methylotrophs , 1982 .

[84]  Soyoung Park,et al.  The effect of various environmental and design parameters on methane oxidation in a model biofilter , 2002, Waste management & research : the journal of the International Solid Wastes and Public Cleansing Association, ISWA.

[85]  Frank Neese,et al.  THE ELECTRONIC STRUCTURE OF CUA : A NOVEL MIXED-VALENCE DINUCLEAR COPPER ELECTRON-TRANSFER CENTER , 1996 .

[86]  D. Leak,et al.  Copper stress underlies the fundamental change in intracellular location of methane mono-oxygenase in methane-oxidizing organisms: Studies in batch and continuous cultures , 2004, Biotechnology Letters.

[87]  E. Boyd,et al.  The Membrane-Associated Methane Monooxygenase (pMMO) and pMMO-NADH:Quinone Oxidoreductase Complex from Methylococcus capsulatus Bath , 2003, Journal of bacteriology.

[88]  Mindy I. Davis,et al.  Geometric and electronic structure/function correlations in non-heme iron enzymes. , 2000, Chemical reviews.

[89]  L. Sayavedra-Soto,et al.  Molecular biology and biochemistry of ammonia oxidation by Nitrosomonas europaea , 2002, Archives of Microbiology.

[90]  J. Semrau,et al.  Characterization of methanotrophic bacteria on the basis of intact phospholipid profiles. , 2000, FEMS microbiology letters.

[91]  P. Epstein,et al.  Climate change and infectious disease: stormy weather ahead? , 2002, Epidemiology.

[92]  M. Lidstrom,et al.  Expression of Individual Copies ofMethylococcus capsulatus Bath Particulate Methane Monooxygenase Genes , 2001, Journal of bacteriology.

[93]  R. Periana,et al.  Platinum catalysts for the high-yield oxidation of methane to a methanol derivative , 1998, Science.

[94]  J. Zahn,et al.  Membrane-associated methane monooxygenase from Methylococcus capsulatus (Bath) , 1996, Journal of bacteriology.

[95]  D. Arp,et al.  Interaction of Ammonia Monooxygenase from Nitrosomonas europaea with Alkanes, Alkenes, and Alkynes , 1988, Applied and environmental microbiology.

[96]  L. Sayavedra-Soto,et al.  Differential regulation of amoA and amoB gene copies in Nitrosomonas europaea. , 2000, FEMS microbiology letters.

[97]  H. J. Kim,et al.  Copper-Binding Compounds from Methylosinus trichosporium OB3b , 1998, Journal of bacteriology.

[98]  K. Gerdes,et al.  Copper‐dependent reciprocal transcriptional regulation of methane monooxygenase genes in Methylococcus capsulatus and Methylosinus trichosporium , 1997, Molecular microbiology.

[99]  K. Kovács,et al.  A novel thermophilic methane-oxidising γ-Proteobacterium , 1999 .

[100]  K. Kovács,et al.  Genes involved in the copper-dependent regulation of soluble methane monooxygenase of Methylococcus capsulatus (Bath): cloning, sequencing and mutational analysis. , 2003, Microbiology.

[101]  T. Wood,et al.  Metal ions and chloramphenicol inhibition of soluble methane monooxygenase from Methylosinus trichosporium OB3b , 1996, Applied Microbiology and Biotechnology.

[102]  D. Bourne,et al.  Molecular methods for the study of methanotroph ecology , 1998 .

[103]  G. E. Speitel,et al.  Phenotypic characterization of copper-resistant mutants of Methylosinus trichosporium OB3b , 1993, Applied and environmental microbiology.

[104]  H. Dalton,et al.  Solubilisation of methane monooxygenase from Methylococcus capsulatus (Bath). , 1989, European journal of biochemistry.

[105]  H. Dalton,et al.  The soluble methane mono-oxygenase of Methylococcus capsulatus (Bath). Its ability to oxygenate n-alkanes, n-alkenes, ethers, and alicyclic, aromatic and heterocyclic compounds. , 1977, The Biochemical journal.

[106]  G. Salmond,et al.  Molecular analysis of methane monooxygenase from Methylococcus capsulatus (Bath) , 2004, Archives of Microbiology.

[107]  H. Dalton,et al.  Copper ions as inhibitors of protein C of soluble methane monooxygenase of Methylococcus capsulatus (Bath). , 1985, European journal of biochemistry.

[108]  M. Collins,et al.  Type 2 Cu2+ in pMMO from Methylomicrobium album BG8. , 1999, Biophysical journal.

[109]  Yu‐Ju Chen,et al.  Production of High-Quality Particulate Methane Monooxygenase in High Yields from Methylococcus capsulatus (Bath) with a Hollow-Fiber Membrane Bioreactor , 2003, Journal of bacteriology.