Skip to main content

The Biochemistry of Methane Monooxygenases

  • Chapter
  • First Online:
Methanotrophs

Part of the book series: Microbiology Monographs ((MICROMONO,volume 32))

Abstract

Selective methane (CH4) oxidation is extremely difficult chemistry. Methane monooxygenases (MMOs ) facilitate the biological conversion of CH4 into methanol in methanotrophs under ambient temperatures and pressures . Methanotrophs typically express the membrane-bound particulate form of MMO (pMMO ), but the soluble form of MMO (sMMO ) is often expressed under copper-limiting conditions. Numerous biochemical and biophysical approaches have been explored to elucidate the mechanisms of pMMO and sMMO over the past four decades, especially to examine the structures and the functional roles of the active sites . In this chapter, the biochemistry, including structural and functional features of MMOs, will be described. We first summarize the biochemical/biophysical studies that have led to the discovery of a unique tricopper cluster as the catalytic site in pMMO and culminated in the successful development of a biomimetic catalyst capable of mediating efficient CH4 oxidation at room temperature. We then review the spectroscopic, kinetic, and structural studies that have contributed to clarification of the catalytic mechanisms near the non-heme diiron active sites in the hydroxylase of sMMO, as well as the roles played by the regulatory protein and the reductase in this chemistry.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Anthony C (1982) The biochemistry of methylotrophs. Academic, London

    Google Scholar 

  • Bailey LJ, McCoy JG, Phillips GN, Fox BG (2008) Structural consequences of effector protein complex formation in a diiron hydroxylase. Proc Natl Acad Sci U S A 105:19194–19198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balasubramanian R, Smith SM, Rawat S, Yatsunyk LA, Stemmler TL, Rosenzweig AC (2010) Oxidation of methane by a biological dicopper centre. Nature 465:115–119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banerjee R, Proshlyakov Y, Lipscomb JD, Proshlyakov DA (2015) Structure of the key species in the enzymatic oxidation of methane to methanol. Nature 518:431–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Basu P, Katterle B, Andersson KK, Dalton H (2003) The membrane-associated form of methane mono-oxygenase from Methylococcus capsulatus (Bath) is a copper/iron protein. Biochem J 369:417–427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blanksby SJ, Ellison GB (2003) Bond dissociation energies of organic molecules. Acc Chem Res 36:255–263

    Article  CAS  PubMed  Google Scholar 

  • Blazyk JL, Gassner GT, Lippard SJ (2005) Intermolecular electron-transfer reactions in soluble methane monooxygenase: a role for hysteresis in protein function. J Am Chem Soc 127:17364–17376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blazyk JL, Lippard SJ (2002) Expression and characterization of ferredoxin and flavin adenine dinucleotide binding domains of the reductase component of soluble methane monooxygenase from Methylococcus capsulatus (Bath). Biochemistry 41:15780–15794

    Article  CAS  PubMed  Google Scholar 

  • Blazyk JL, Lippard SJ (2004) Domain engineering of the reductase component of soluble methane monooxygenase from Methylococcus capsulatus (Bath). J Biol Chem 279:5630–5640

    Article  CAS  PubMed  Google Scholar 

  • Cao L, Caldararu O, Rosenzweig AC, Ryde U (2018) Quantum refinement does not support dinuclear copper sites in crystal structures of particulate methane monooxygenase. Angew Chem Int Ed 57:162–166

    Article  CAS  Google Scholar 

  • Cardy DL, Laidler V, Salmond GP, Murrell JC (1991) The methane monooxygenase gene cluster of Methylosinus trichosporium: cloning and sequencing of the mmoC gene. Arch Microbiol 156:477–483

    Article  CAS  PubMed  Google Scholar 

  • Castillo RG, Banerjee R, Allpress CJ, Rohde GT, Bill E, Que L, Lipscomb JD, DeBeer S (2017) High-energy-resolution fluorescence-detected X-ray absorption of the Q intermediate of soluble methane monooxygenase. J Am Chem Soc 139:18024–18033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan SI, Nguyen HHT, Shiemke AK, Lidstrom ME (1993) The copper ions in the membrane-associated methane monooxygenase. In: Karlin KD, Tyeklar Z (eds) Bioinorganic chemistry of copper. Chapman and Hall, New York

    Google Scholar 

  • Chan SI, Chen KHC, Yu SSF, Chen CL, Kuo SSJ (2004) Toward delineating the structure and function of the particulate methane monooxygenase from methanotrophic bacteria. Biochemistry 43:4421–4430

    Article  CAS  PubMed  Google Scholar 

  • Chan SI, Wang VCC, Lai JCH, Yu SSF, Chen PPY, Chen KHC, Chen CL, Chan MK (2007) Redox potentiometry studies of particulate methane monooxygenase: support for a trinuclear copper cluster active site. Angew Chem Int Ed 46:1992–1994

    Article  CAS  Google Scholar 

  • Chan SI, Yu SSF (2008) Controlled oxidation of hydrocarbons by the membrane-bound methane monooxygenase: the case for a tricopper cluster. Acc Chem Res 41:969–979

    Article  CAS  PubMed  Google Scholar 

  • Chan SI, Nguyen HHT, Chen KHC, Yu SSF (2011) Overexpression and purification of the particulate methane monooxygenase from Methylococcus capsulatus (Bath). In: Rosenzweig AC, Ragsdale SW (eds) Methods in methane metabolism, methods in enzymology, vol 495. Academic, Burlington, MA, pp 177–193

    Chapter  Google Scholar 

  • Chan SI, Lu YJ, Nagababu P, Maji S, Hung MC, Lee MM, Hsu IJ, Minh PD, Lai JCH, Ng KY, Ramalingam S, Yu SSF, Chan MK (2013) Efficient oxidation of methane to methanol by dioxygen mediated by tricopper clusters. Angew Chem Int Ed 52:3731–3735

    Article  CAS  Google Scholar 

  • Chang SL, Wallar BJ, Lipscomb JD, Mayo KH (1999) Solution structure of component B from methane monooxygenase derived through heteronuclear NMR and molecular modeling. Biochemistry 38:5799–5812

    Article  CAS  PubMed  Google Scholar 

  • Chatwood LL, Muller J, Gross JD, Wagner G, Lippard SJ (2004) NMR structure of the flavin domain from soluble methane monooxygenase reductase from Methylococcus capsulatus (Bath). Biochemistry 43:11983–11991

    Article  CAS  PubMed  Google Scholar 

  • Chen KHC, Chen CL, Tseng CF, Yu SSF, Ke SC, Lee JF, Nguyen HT, Elliott SJ, Alben JO, Chan SI (2004) The copper clusters in the particulate methane monooxygenase (pMMO) from Methylococcus capsulatus (Bath). J Chin Chem Soc 51:1081–1098

    Article  CAS  Google Scholar 

  • Chen PPY, Nagababu P, Yu SSF, Chan SI (2014) Development of the tricopper cluster as a catalyst for the efficient conversion of methane into MeOH. ChemCatChem 6:429–437

    Article  CAS  Google Scholar 

  • Chidambaram-Padmavathy K, Oblulisamy PK, Heimann K (2015) Role of copper and iron in methane oxidation and bacterial biopolymer accumulation. Eng Life Sci 15:387–399

    Article  CAS  Google Scholar 

  • Choi DW, Kunz RC, Boyd ES, Semrau JD, Antholine WE, Han JI, Zahn JA, Boyd JM, de la Mora AM, DiSpirito AA (2003) The membrane-associated methane monooxygenase (pMMO) and pMMO-NADH: quinone oxidoreductase complex from Methylococcus capsulatus (Bath). J Bacteriol 185:5755–5764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colby J, Stirling DI, Dalton H (1977) Soluble methane mono-oxygenase of Methylococcus capsulatus (Bath). Its ability to oxygenate n-alkanes, n-alkenes, ethers, and alicyclic, aromatic and heterocyclic-compounds. Biochem J 165:395–402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davydov A, Davydov R, Graslund A, Lipscomb JD, Andersson KK (1997) Radiolytic reduction of methane monooxygenase dinuclear iron cluster at 77 K - EPR evidence for conformational change upon reduction or binding of component B to the diferric state. J Biol Chem 272:7022–7026

    Article  CAS  PubMed  Google Scholar 

  • Davydov R, Hoffman BM, Valentine AM, Lippard SJ, Sligar SG, Ikeda-Saito M (1999a) EPR and ENDOR studies on cryoreduced metalloproteins. J Inorg Biochem 74:110

    Google Scholar 

  • Davydov R, Valentine AM, Komar-Panicucci S, Hoffman BM, Lippard SJ (1999b) An EPR study of the dinuclear iron site in the soluble methane monooxygenase from Methylococcus capsulatus (Bath) reduced by one electron at 77 K: the effects of component interactions and the binding of small molecules to the diiron(III) center. Biochemistry 38:4188–4197

    Article  CAS  PubMed  Google Scholar 

  • Deeth RJ, Dalton H (1998) Methane activation by methane monooxygenase: free radicals, Fe-C bonding, substrate dependent pathways and the role of the regulatory protein. J Biol Inorg Chem 3:302–306

    Article  CAS  Google Scholar 

  • DeRose VJ, Liu KE, Kurtz DM, Hoffman BM, Lippard SJ (1993) Proton ENDOR identification of bridging hydroxide ligands in mixed-valent diiron centers of proteins: methane monooxygenase and semimet azidohemerythrin. J Am Chem Soc 115:6440–6441

    Article  CAS  Google Scholar 

  • Dewitt JG, Bentsen JG, Rosenzweig AC, Hedman B, Green J, Pilkington S, Papaefthymiou GC, Dalton H, Hodgson KO, Lippard SJ (1991) X-ray absorption, moessbauer, and EPR studies of the dinuclear iron center in the hydroxylase component of methane monooxygenase. J Am Chem Soc 113:9219–9235

    Article  CAS  Google Scholar 

  • Elango N, Radhakrishnan R, Froland WA, Wallar BJ, Earhart CA, Lipscomb JD, Ohlendorf DH (1997) Crystal structure of the hydroxylase component of methane monooxygenase from Methylosinus trichosporium OB3b. Protein Sci 6:556–568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elliott SJ, Zhu M, Tso L, Nguyen HHT, Yip JHK, Chan SI (1997) Regio- and stereoselectivity of particulate methane monooxygenase from Methylococcus capsulatus (Bath). J Am Chem Soc 119:9949–9955

    Article  CAS  Google Scholar 

  • Feig AL, Lippard SJ (1994) Reactions of non-heme iron(II) centers with dioxygen in biology and chemistry. Chem Rev 94:759–805

    Article  CAS  Google Scholar 

  • Fox BG, Froland WA, Dege JE, Lipscomb JD (1989) Methane monooxygenase from Methylosinus trichosporium OB3b - purification and properties of a three-component system with high specific activity from a type II methanotroph. J Biol Chem 264:10023–10033

    CAS  PubMed  Google Scholar 

  • Fox BG, Liu Y, Dege JE, Lipscomb JD (1991) Complex formation between the protein components of methane monooxygenase from Methylosinus trichosporium OB3b - identification of sites of component interaction. J Biol Chem 266:540–550

    CAS  PubMed  Google Scholar 

  • Fox BG, Surerus KK, Munck E, Lipscomb JD (1988) Evidence for a μ-oxo-bridged binuclear iron cluster in the hydroxylase component of methane monooxygenase - Mössbauer and EPR studies. J Biol Chem 263:10553–10556

    CAS  PubMed  Google Scholar 

  • Froland WA, Andersson KK, Lee SK, Liu Y, Lipscomb JD (1992) Methane monooxygenase component B and reductase alter the regioselectivity of the hydroxylase component-catalyzed reactions - a novel role for protein-protein interactions in an oxygenase mechanism. J Biol Chem 267:17588–17597

    CAS  PubMed  Google Scholar 

  • Gassner GT, Lippard SJ (1999) Component interactions in the soluble methane monooxygenase system from Methylococcus capsulatus (Bath). Biochemistry 38:12768–12785

    Article  CAS  PubMed  Google Scholar 

  • Green J, Dalton H (1989) A stopped-flow kinetic study of soluble methane mono-oxygenase from Methylococcus capsulatus (Bath). Biochem J 259:167–172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hakemian AS, Kondapalli KC, Telser J, Hoffman BM, Stemmler TL, Rosenzweig AC (2008) The metal centers of particulate methane monooxygenase from Methylosinus trichosporium OB3b. Biochemistry 47:6793–6801

    Article  CAS  PubMed  Google Scholar 

  • Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jasniewski AJ, Que L (2018) Dioxygen activation by nonheme diiron enzymes: diverse dioxygen adducts, high-valent intermediates, and related model complexes. Chem Rev 118:2554–2592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kao WC, Chen YR, Yi EC, Lee H, Tian Q, Wu KM, Tsai SF, Yu SSF, Chen YJ, Aebersold R, Chan SI (2004) Quantitative proteomic analysis of metabolic regulation by copper ions in Methylococcus capsulatus (Bath). J Biol Chem 279:51554–51560

    Article  CAS  PubMed  Google Scholar 

  • Kim HJ, Graham DW, DiSpirito AA, Alterman MA, Galeva N, Larive CK, Asunskis D, Sherwood PMA (2004) Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria. Science 305:1612–1615

    Article  CAS  PubMed  Google Scholar 

  • Kopp DA, Gassner GT, Blazyk JL, Lippard SJ (2001) Electron-transfer reactions of the reductase component of soluble methane monooxygenase from Methylococcus capsulatus (Bath). Biochemistry 40:14932–14941

    Article  CAS  PubMed  Google Scholar 

  • Lee SJ, McCormick MS, Lippard SJ, Cho US (2013) Control of substrate access to the active site in methane monooxygenase. Nature 494:380–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SK, Lipscomb JD (1999) Oxygen activation catalyzed by methane monooxygenase hydroxylase component: proton delivery during the O–O bond cleavage steps. Biochemistry 38:4423–4432

    Article  CAS  PubMed  Google Scholar 

  • Lieberman RL, Rosenzweig AC (2005) Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane. Nature 434:177–182

    Article  CAS  PubMed  Google Scholar 

  • Lipscomb JD (1994) Biochemistry of the soluble methane monooxygenase. Annu Rev Microbiol 48:371–399

    Article  CAS  PubMed  Google Scholar 

  • Lipscomb JD, Lee SK, Nesheim JC, Froland WA, Fox BG, Munck E (1994) Reactive intermediates in the methane monooxygenase catalyzed oxidation of methane and other hydrocarbons. Abstr Pap Am Chem Soc 207:273

    Google Scholar 

  • Liu CC, Mou CY, Yu SSF, Chan SI (2016) Heterogeneous formulation of the tricopper complex for efficient catalytic conversion of methane into methanol at ambient temperature and pressure. Energy Environ Sci 9:1361–1374

    Article  CAS  Google Scholar 

  • Liu CC, Janmanchi D, Wen DR, Oung JN, Mou CY, Yu SSF, Chan SI (2018) Catalytic oxidation of light alkanes mediated at room temperature by a tricopper cluster complex immobilized in mesoporous silica nanoparticles. ACS Sustain Chem Eng 6(4):5431–5440

    Article  CAS  Google Scholar 

  • Liu KE, Valentine AM, Wang DL, Huynh BH, Edmondson DE, Salifoglou A, Lippard SJ (1995a) Kinetic and spectroscopic characterization of intermediates and component interactions in reactions of methane monooxygenase from Methylococcus capsulatus (Bath). J Am Chem Soc 117:10174–10185

    Article  CAS  Google Scholar 

  • Liu KE, Wang DL, Huynh BH, Edmondson DE, Salifoglou A, Lippard SJ (1994) Spectroscopic detection of intermediates in the Reaction of dioxygen with the reduced methane monooxygenase/hydroxylase from Methylococcus capsulatus (Bath). J Am Chem Soc 116:7465–7466

    Article  CAS  Google Scholar 

  • Liu Y, Nesheim JC, Lee SK, Lipscomb JD (1995b) Gating effects of component B on oxygen activation by the methane monooxygenase hydroxylase component. J Biol Chem 270:24662–24665

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Nesheim JC, Paulsen KE, Stankovich MT, Lipscomb JD (1997) Roles of the methane monooxygenase reductase component in the regulation of catalysis. Biochemistry 36:5223–5233

    Article  CAS  PubMed  Google Scholar 

  • Lloyd JS, Bhambra A, Murrell JC, Dalton H (1997) Inactivation of the regulatory protein B of soluble methane monooxygenase from Methylococcus capsulatus (Bath) by proteolysis can be overcome by a Gly to Gln modification. Eur J Biochem 248:72–79

    Article  CAS  PubMed  Google Scholar 

  • Lu YJ, Hung MC, Chang BTA, Lee TL, Lin ZH, Tsai IK, Chen YS, Chang CS, Tsai YF, Chen KHC, Chan SI, Yu SSF (2019) The PmoB subunit of particulate methane monooxygenase (pMMO) in Methylococcus capsulatus (Bath): the CuI sponge and its function. J Inorg Biochem 196:110691

    Article  CAS  PubMed  Google Scholar 

  • Lund J, Woodland MP, Dalton H (1985) Electron transfer reactions in the soluble methane monooxygenase of Methylococcus capsulatus (Bath). Eur J Biochem 147:297–305

    Article  CAS  PubMed  Google Scholar 

  • Maji S, Lee JCM, Lu YJ, Chen CL, Hung MC, Chen PPY, Yu SSF, Chan SI (2012) Dioxygen activation of a trinuclear CuICuICuI cluster capable of mediating facile oxidation of organic substrates: competition between O-atom transfer and abortive intercomplex reduction. Chem Eur J 18:3955–3968

    Article  CAS  PubMed  Google Scholar 

  • McCormick MS, Lippard SJ (2011) Analysis of substrate access to active sites in bacterial multicomponent monooxygenase hydroxylases: X-ray crystal structure of xenon-pressurized phenol hydroxylase from Pseudomonas sp. OX1. Biochemistry 50:11058–11069

    Article  CAS  PubMed  Google Scholar 

  • Merkx M, Kopp DA, Sazinsky MH, Blazyk JL, Muller J, Lippard SJ (2001) Dioxygen activation and methane hydroxylation by soluble methane monooxygenase: a tale of two irons and three proteins. Angew Chem Int Ed 40:2782–2807

    Article  CAS  Google Scholar 

  • Merkx M, Lippard SJ (2002) Why OrfY? Characterization of MMOD, a long overlooked component of the soluble methane monooxygenase from Methylococcus capsulatus (Bath). J Biol Chem 277:5858–5865

    Article  CAS  PubMed  Google Scholar 

  • Muller J, Lugovskoy AA, Wagner G, Lippard SJ (2002) NMR structure of the [2Fe-2S] ferredoxin domain from soluble methane monooxygenase reductase and interaction with its hydroxylase. Biochemistry 41:42–51

    Article  PubMed  CAS  Google Scholar 

  • Murray LJ, Lippard SJ (2007) Substrate trafficking and dioxygen activation in bacterial multicomponent monooxygenases. Acc Chem Res 40:466–474

    Article  CAS  PubMed  Google Scholar 

  • Murrell JC, McDonald IR, Gilbert B (2000) Regulation of expression of methane monooxygenases by copper ions. Trends Microbiol 8:221–225

    Article  CAS  PubMed  Google Scholar 

  • Myronova N, Kitmitto A, Collins RF, Miyaji A, Dalton H (2006) Three-dimensional structure determination of a protein supercomplex that oxidizes methane to formaldehyde in Methylococcus capsulatus (Bath). Biochemistry 45:11905–11914

    Article  CAS  PubMed  Google Scholar 

  • Nagababu P, Yu SSF, Maji S, Ramu R, Chan SI (2014) Developing an efficient catalyst for controlled oxidation of small alkanes under ambient conditions. Cat Sci Technol 4:930–935

    Article  CAS  Google Scholar 

  • Nesheim JC, Lipscomb JD (1996) Large kinetic isotope effects in methane oxidation catalyzed by ethane monooxygenase: evidence for C–H bond cleavage in a reaction cycle intermediate. Biochemistry 35:10240–10247

    Article  CAS  PubMed  Google Scholar 

  • Ng KY, Tu LC, Wang YS, Chan SI, Yu SSF (2008) Probing the hydrophobic pocket of the active site in the particulate methane monooxygenase (pMMO) from Methylococcus capsulatus (Bath) by variable stereoselective alkane hydroxylation and olefin epoxidation. Chembiochem 9:1116–1123

    Article  CAS  PubMed  Google Scholar 

  • Nguyen HHT, Shiemke AK, Jacobs SJ, Hales BJ, Lidstrom ME, Chan SI (1994) The nature of the copper ions in the membranes containing the particulate methane monooxygenase from Methylococcus capsulatus (Bath). J Biol Chem 69:14995–15005

    Google Scholar 

  • Nguyen HHT, Nakagawa KH, Hedman B, Elliott SJ, Lidstrom ME, Hodgson KO, Chan SI (1996) 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. J Am Chem Soc 118:12766–12776

    Article  CAS  Google Scholar 

  • Nguyen HHT, Elliott SJ, Yip JHK, Chan SI (1998) The particulate methane monooxygenase from Methylococcus capsulatus (Bath) is a novel copper-containing three-subunit enzyme—isolation and characterization. J Biol Chem 273:7957–7966

    Article  CAS  PubMed  Google Scholar 

  • Pham MD, Yu SSF, Han CC, Chan SI (2013) Improved mass spectrometric analysis of membrane proteins based on rapid and versatile sample preparation on nanodiamond particles. Anal Chem 85:6748–6755

    Article  CAS  PubMed  Google Scholar 

  • Pham MD, Lin YP, Vuong QV, Nagababu P, Chang BTA, Ng KY, Chen CH, Han CC, Chen CH, Li MS, Yu SSF, Chan SI (2015) Inactivation of the particulate methane monooxygenase (pMMO) in Methylococcus capsulatus (Bath) by acetylene. Biochim Biophys Acta Proteins Proteomics 1854:1842–1852

    Article  CAS  Google Scholar 

  • Pulver S, Froland WA, Fox BG, Lipscomb JD, Solomon EI (1993) Spectroscopic studies of the coupled binuclear non-heme iron active site in the fully reduced hydroxylase component of methane monooxygenase: comparison to deoxy and deoxy-azide hemerythrin. J Am Chem Soc 115:12409–12422

    Article  CAS  Google Scholar 

  • Pulver S, Froland WA, Fox BG, Lipscomb JD, Solomon EI (1994) Spectroscopic studies of the coupled binuclear non-heme iron active site in the fully reduced hydroxylase component of methane monooxygenase: comparison to deoxy and deoxy-azide hemerythrin. J Am Chem Soc 116:4529–4529

    Article  CAS  Google Scholar 

  • Rosenzweig AC, Brandstetter H, Whittington DA, Nordlund P, Lippard SJ, Frederick CA (1997) Crystal structures of the methane monooxygenase hydroxylase from Methylococcus capsulatus (Bath): implications for substrate gating and component interactions. Proteins Struct Funct Genet 29:141–152

    Article  CAS  PubMed  Google Scholar 

  • Rosenzweig AC, Frederick CA, Lippard SJ, Nordlund P (1993) Crystal structure of a bacterial non-haem iron hydroxylase that catalyses the biological oxidation of methane. Nature 366:537–543

    Article  CAS  PubMed  Google Scholar 

  • Rosenzweig AC, Nordlund P, Takahara PM, Frederick CA, Lippard SJ (1995) Geometry of the soluble methane monooxygenase catalytic diiron center in two oxidation states. Chem Biol 2:409–418

    Article  CAS  PubMed  Google Scholar 

  • Sazinsky MH, Dunten PW, McCormick MS, DiDonato A, Lippard SJ (2006) X-ray structure of a hydroxylase-regulatory protein complex from a hydrocarbon-oxidizing multicomponent monooxygenase, Pseudomonas sp. OX1 phenol hydroxylase. Biochemistry 45:15392–15404

    Article  CAS  PubMed  Google Scholar 

  • Sazinsky MH, Lippard SJ (2006) Correlating structure with function in bacterial multicomponent monooxygenases and related diiron proteins. Acc Chem Res 39:558–566

    Article  CAS  PubMed  Google Scholar 

  • Semrau JD, DiSpirito AA, Yoon S (2010) Methanotrophs and copper. FEMS Microbiol Rev 34:496–531

    Article  CAS  PubMed  Google Scholar 

  • Shindell DT, Faluvegi G, Koch DM, Schmidt GA, Unger N, Bauer SE (2009) Improved attribution of climate forcing to emissions. Science 326:716–718

    Article  CAS  PubMed  Google Scholar 

  • Shinohara Y, Uchiyama H, Yagi O, Kusakabe I (1998) Purification and characterization of component B of a soluble methane monooxygenase from Methylocystis sp. M. J Ferment Bioeng 85:37–42

    Article  CAS  Google Scholar 

  • Shu LJ, Nesheim JC, Kauffmann K, Munck E, Lipscomb JD, Que L (1997) An Fe2 IVO2 diamond core structure for the key intermediate Q of methane monooxygenase. Science 275:515–518

    Article  CAS  PubMed  Google Scholar 

  • Sirajuddin S, Barupala D, Helling S, Marcus K, Stemmler TL, Rosenzweig AC (2014) Effects of zinc on particulate methane monooxygenase activity and structure. J Biol Chem 289:21782–21794

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith SM, Rawat S, Telser J, Hoffman BM, Stemmler TL, Rosenzweig AC (2011) Crystal structure and characterization of particulate methane monooxygenase from Methylocystis species Strain M. Biochemistry 50:10231–10240

    Article  CAS  PubMed  Google Scholar 

  • Stafford GP, Scanlan J, McDonald IR, Murrell JC (2003) rpoN, mmoR and mmoG, genes involved in regulating the expression of soluble methane monooxygenase in Methylosinus trichosporium OB3b. Microbiology 149:1771–1784

    Article  CAS  PubMed  Google Scholar 

  • Stainthorpe AC, Lees V, Salmond GPC, Dalton H, Murrell JC (1990) The methane monooxygenase gene cluster of Methylococcus capsulatus (Bath). Gene 91:27–34

    Article  CAS  PubMed  Google Scholar 

  • Stein LY, Yoon S, Semrau JD, DiSpirito AA, Crombie A, Murrell JC, Vuilleumier S, Kalyuzhnaya MG, den Camp HJMO, Bringel F, Bruce D, Cheng JF, Copeland A, Goodwin L, Han SS, Hauser L, Jetten MSM, Lajus A, Land ML, Lapidus A, Lucas S, Médigue C, Pitluck S, Woyke T, Zeytun A, Klotz MG (2010) Genome sequence of the obligate methanotroph Methylosinus trichosporium Strain OB3b. J Bacteriol 192:6497–6498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stolyar S, Costello AM, Peeples TL, Lidstrom ME (1999) Role of multiple gene copies in particulate methane monooxygenase activity in the methane-oxidizing bacterium Methylococcus capsulatus Bath. Microbiology 145:1235–1244

    Article  CAS  PubMed  Google Scholar 

  • Thomann H, Bernardo M, McCormick JM, Pulver S, Andersson KK, Lipscomb JD, Solomon EI (1993) Pulsed EPR studies of mixed valent [Fe(II)Fe(III)] forms of hemerythrin and methane monooxygenase: evidence for a hydroxide bridge. J Am Chem Soc 115:8881–8882

    Article  CAS  Google Scholar 

  • Tinberg CE, Lippard SJ (2009) Revisiting the mechanism of dioxygen activation in soluble methane monooxygenase from M. capsulatus (Bath): evidence for a multi-step, proton-dependent reaction pathway. Biochemistry 48:12145–12158

    Article  CAS  PubMed  Google Scholar 

  • Tinberg CE, Lippard SJ (2010) Oxidation reactions performed by soluble methane monooxygenase hydroxylase intermediates Hperoxo and Q proceed by distinct mechanisms. Biochemistry 49:7902–7912

    Article  CAS  PubMed  Google Scholar 

  • Tinberg CE, Lippard SJ (2011) Dioxygen activation in soluble methane monooxygenase. Acc Chem Res 44:280–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trotsenko YA, Khmelenina VN (2002) Biology of extremophilic and extremotolerant methanotrophs. Arch Microbiol 177:123–131

    Article  CAS  PubMed  Google Scholar 

  • Trotsenko YA, Murrell JC (2008) Metabolic aspects of aerobic obligate methanotrophy. Adv Appl Microbiol 63:183–229

    Article  CAS  PubMed  Google Scholar 

  • Vinchurkar MS, KHC C, SSF Y, Kuo SJ, Chiu HC, Chien SH, Chan SI (2004) Polarized ATR-FTIR spectroscopy of the membrane-embedded domains of the particulate methane monooxygenase. Biochemistry 43:13283–13292

    Article  CAS  PubMed  Google Scholar 

  • Wallar BJ, Lipscomb JD (1996) Dioxygen activation by enzymes containing binuclear non-heme iron clusters. Chem Rev 96:2625–2657

    Article  CAS  PubMed  Google Scholar 

  • Wallar BJ, Lipscomb JD (2001) Methane monooxygenase component B mutants alter the kinetics of steps throughout the catalytic cycle. Biochemistry 40:2220–2233

    Article  CAS  PubMed  Google Scholar 

  • Walters KJ, Gassner GT, Lippard SJ, Wagner G (1999) Structure of the soluble methane monooxygenase regulatory protein B. Proc Natl Acad Sci U S A 96:7877–7882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang VCC, Maji S, Chen PPY, Lee HK, Yu SSF, Chan SI (2017) Alkane oxidation: methane monooxygenases, related enzymes, and their biomimetics. Chem Rev 117:8574–8621

    Article  CAS  PubMed  Google Scholar 

  • Wang WX, Iacob RE, Luoh RP, Engen JR, Lippard SJ (2014) Electron transfer control in soluble methane monooxygenase. J Am Chem Soc 136:9754–9762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang WX, Liang AD, Lippard SJ (2015) Coupling oxygen consumption with hydrocarbon oxidation in bacterial multicomponent monooxygenases. Acc Chem Res 48:2632–2639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang WX, Lippard SJ (2014) Diiron oxidation state control of substrate access to the active site of soluble methane monooxygenase mediated by the regulatory component. J Am Chem Soc 136:2244–2247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ward N, Larsen O, Sakwa J, Bruseth L, Khouri H, Durkin AS, Dimitrov G, Jiang LX, Scanlan D, Kang KH, Lewis M, Nelson KE, Methé B, Wu M, Heidelberg JF, Paulsen IA, Fouts D, Ravel J, Tettlin H, Ren Q, Read T, DeBoy RT, Seshadri R, Salzberg SL, Jensen HB, Birkeland NK, Nelson WC, Dodson RJ, Grindhaug SH, Holt I, Eidhammer I, Jonasen I, Vanaken S, Utterback T, Feldblyum TV, Fraser CM, Lillehaug JR, Eisen JA (2004) Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2:1616–1628

    CAS  Google Scholar 

  • Whittington DA, Lippard SJ (2001) Crystal structures of the soluble methane monooxygenase hydroxylase from Methylococcus capsulatus (Bath) demonstrating geometrical variability at the dinuclear iron active site. J Am Chem Soc 123:827–838

    Article  CAS  PubMed  Google Scholar 

  • Whittington DA, Rosenzweig AC, Frederick CA, Lippard SJ (2001a) Xenon and halogenated alkanes track putative substrate binding cavities in the soluble methane monooxygenase hydroxylase. Biochemistry 40:3476–3482

    Article  CAS  PubMed  Google Scholar 

  • Whittington DA, Sazinsky MH, Lippard SJ (2001b) X-ray crystal structure of alcohol products bound at the active site of soluble methane monooxygenase hydroxylase. J Am Chem Soc 123:1794–1795

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson B, Zhu M, Priestley ND, Nguyen HHT, Morimoto H, Williams PG, Chan SI, Floss HG (1996) A concerted mechanism for ethane hydroxylation by the particulate methane monooxygenase from Methylococcus capsulatus (Bath). J Am Chem Soc 118:921–922

    Article  CAS  Google Scholar 

  • Yu SSF, Chen KHC, Tseng MYH, Wang YS, Tseng CF, Chen YJ, Huang DS, Chan SI (2003a) Production of high-quality particulate methane monooxygenase in high yields from Methylococcus capsulatus (Bath) with a hollow-fiber membrane bioreactor. J Bacteriol 185:5915–5924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu SSF, Wu LY, Chen KHC, Luo WI, Huang DS, Chan SI (2003b) The stereospecific hydroxylation of [2, 2-2H2]butane and chiral dideuteriobutanes by the particulate methane monooxygenase from Methylococcus capsulatus (Bath). J Biol Chem 278:40658–40669

    Article  CAS  PubMed  Google Scholar 

  • Yu SSF, Ji CZ, Wu YP, Lee TL, Lai CH, Lin SC, Yang ZL, Wang VCC, Chen KHC, Chan SI (2007) The C-terminal aqueous-exposed domain of the 45 kDa subunit of the particulate methane monooxygenase in Methylococcus capsulatus (Bath) is a Cu(I) sponge. Biochemistry 46:13762–13774

    Article  CAS  PubMed  Google Scholar 

  • Zahn JA, DiSpirito AA (1996) Membrane-associated methane monooxygenase from Methylococcus capsulatus (Bath). J Bacteriol 178:1018–1029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Seung Jae Lee .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Chan, S.I., Lee, S.J. (2019). The Biochemistry of Methane Monooxygenases. In: Lee, E. (eds) Methanotrophs. Microbiology Monographs, vol 32. Springer, Cham. https://doi.org/10.1007/978-3-030-23261-0_3

Download citation

Publish with us

Policies and ethics