Abstract
Methane-oxidizing bacteria (methanotrophs) are a unique group of aerobic bacteria that can gain all of their carbon and energy requirements from methane. The enzymes that catalyze the first step in the bacterial methane oxidation pathway, the oxidation of methane to methanol, are called methane monooxygenases. These are remarkable enzymes because methane is chemically very stable, and to convert methane to methanol chemically requires expensive catalysts, high temperatures, and pressures. There are two types of methane monooxygenase that occur in methanotrophs, a membrane-bound, particulate methane monooxygenase, and a cytoplasmic, soluble methane monooxygenase which belongs to a class of enzymes known as soluble diiron monooxygenases. The expression of these enzymes in methanotrophs is often regulated by the availability of copper. The soluble methane monooxygenase has attracted significant attention and has considerable potential in biocatalysis and bioremediation since it can co-oxidize a very wide range of aliphatic and aromatic compounds, even though methanotrophs themselves do not grow on these compounds. We review here the biochemistry and molecular biology of both the particulate and soluble methane monooxygenases and their biotechnological potential.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Anthony C (1982) The biochemistry of Methylotrophs. Academic, New York
Baani M, Liesack W (2008) Two isoenzymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp SC2. Proc Natl Acad Sci 105:10203–10208
Baik MH, Newcomb M, Friesner RA, Lippard SJ (2003) Mechanistic studies on the hydroxylation of methane by methane monooxygenase. Chem Rev 103:2385–2419
Balasubramanian R, Rosenzweig AC (2008) Copper methanobaction: a molecule whose time has come. Curr Opin Chem Eng 12:245–249
Balasubramanian R, Smith SM, Rawat S, Yatsunyk LA, Stemmler TL, Rosenzweig AC (2010) Oxidation of methane by a biological dicopper center. Nature 465:115–119
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
Bjorck CE, Dobson PD, Pandhal J (2018) Biotechnological conversion of methane to methanol: evaluation of progress and potential. AIMS Bioeng 5:1–38
Borodina E, Nichol T, Dumont MG, Smith TJ, Murrell JC (2007) Mutagenesis of the “leucine gate” to explore the basis of catalytic versatility in soluble methane monooxygenase. Appl Environ Microbiol 73:6460–6467
Cantera S, Muñoz R, Lebrero R, López JC, Rodríguez Y, García-Encina PA (2018) Technologies for the bioconversion of methane into more valuable products. Curr Opin Biotechnol 50:128–135
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 130:168–172
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
Chatwood LL, Muller J, Gross JD, Wagner G, Lippard SJ (2004) Biochemistry 43:11983–11991
Cho U-S, Lee SJ, Kim H, An S, Park YR, Jang H, Park S (2018) MMOD-induced structural changes of hydroxylase in soluble methane monooxygenase. BioRxiv. https://doi.org/10.1101/331512
Choi DW, Antholine WE, Do YS, Semrau JD, Kisting CJ, Kunz RC, Campbell D, Rao V, Hartsel SC, DiSpirito AA (2005) Effect of methanobactin on the activity and electron paramagnetic resonance spectra of the membrane-associated methane monooxygenase in Methylococcus capsulatus Bath. Microbiology 151:3417–3426
Choi DW, Do YS, Zea JC (2006) Spectral and thermodynamic properties of Ag(I), Au(III), Cd(II), Co(II), Fe(III), Hg(II), Mn(II), Ni(II), Pb(II), U(IV), and Zn(II) binding by methanobactin from Methylosinus trichosporium OB3b. J Inorg Biochem 100:2150–2161
Coleman NV, Bui NB, Holmes AJ (2006) Soluble di-iron monooxygenase gene diversity in soils, sediments and ethene enrichments. Environ Microbiol 8:1228–1239
Crombie AT, Murrell JC (2014) Trace-gas metabolic versatility of the facultative methanotroph Methylocella silvestris. Nature 510:148–151
Csaki R, Bodrossy L, Klem J, Murrell JC, Kovacs KL (2003) Genes involved in the copper-dependent regulation of soluble methane monooxygenase of Methylococcus capsulatus (Bath): cloning, sequencing and mutational analysis. Microbiology 149:1785–1795
Dalton H (2005) The Leeuwenhoek lecture 2000. The natural and unnatural history of methane oxidizing bacteria. Philos Trans R Soc Lond B 360:1207–1222
Dedysh SN, Knief C, Dunfield P (2005) Methylocella species are facultatively methanotrophic. J Bacteriol 187:4665–4667
Dedysh SN, Naumoff DG, Vorobev AV, Kyrpides N, Woyke T, Shapiro N, Crombie AT, Murrell JC, Kalyuzhnaya MG, Smirnova AV, Dunfield PF (2015) Draft genome sequence of Methyloferula stellata AR4, an obligate methanotroph possessing only a soluble methane monooxygenase. Genome Announc 3:e01555–e01514
DiSpirito AA, Zahn JA, Graham DW, Kim HJ, Larive CK, Derrick TS, Cox CD, Taylor A (1998) Copper-binding compounds from Methylosinus trichosporium OB3b. J Bacteriol 180:3606–3613
DiSpirito AA, Semrau JD, Murrell JC, Gallagher WH, Dennison C, Vuilleumier S (2016) Methanobactin and the link between copper and bacterial methane oxidation. Microbiol Mol Biol Rev 80:387–409
Elango N, Radhakrishnan R, Froland WA, Wallar BJ, Earhart CA, Lipscomb JD, Ohlendorf DH (1997) Crystal structure of the hydroxylase component of the soluble methane monooxygenase from Methylosinus trichosporium OB3b. Protein Sci 6:556–568
Gu W, Semrau JD (2017) Copper and cerium-regulated gene expression in Methylosinus trichosporium OB3b. Appl Microbiol Biotechnol 101:8499–8516
Gu W, Farhan Ul Haque M, Semrau, JD (2017) Characterization of the role of copCD in copper uptake and the ‘copper-switch’ in Methylosinus trichosporium OB3b. FEMS Microbiol Lett, 364:fnx094.
Hakemian AS, Rosenzweig AC (2007) The biochemistry of methane oxidation. Annu Rev Biochem 76:223–241
Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471
Hazen TC, Chakraborty R, Fleming JM, Gregory IR, Bowman JP, Jimenez L, Zhang D, Pfiffner SM, Brockman FJ, Sayler GS (2009) Use of gene probes to assess the impact and effectiveness of aerobic in situ bioremediation of TCE. Arch Microbiol 91:221–232
Im J, Semrau JD (2011) Pollutant degradation by a Methylocystis strain SB2 grown on ethanol: bioremediation via facultative methanotrophy. FEMS Microbiol Lett 318:137–142
Jasniewski AJ, Que L (2018) Dioxygen activation by nonheme diiron enzymes: diverse dioxygen adducts, high-valent intermediates, and related model complexes. Chem Rev 18:2554–2592
Jin Y, Lipscomb JD (2000) Mechanistic insights into C-H activation from radical clock chemistry: oxidation of substituted methylcyclopropanes catalyzed by soluble methane monooxygenase from Methylosinus trichosporium OB3b. Biochim Biophys Acta 1543:47–59
Kenney GE, Rosenzweig AC (2018) Methanobactins: maintaining copper homeostasis in methanotrophs and beyond. J Biol Chem 293:4606. TM117.000185
Kenney GE, Sadek M, Rosenzweig AC (2016) Copper-responsive gene expression in the methanotroph Methylosinus trichosporium OB3b. Metallomics 8:931–940
Kim HJ, Graham DW, DiSpirito AA, Alterman MA, Galeva N, Larive CK, Asunskis D (2004) Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria. Science 305:1612–1615
Kim HJ, Galeva N, Larive CK, Alterman M, Graham DW (2005) Purification and physical-chemical properties of methanobactin: a chalkophore from Methylosinus trichosporium OB3b. Biochemistry 44:5140–5148
Kitmitto A, Myronova N, Basu P, Dalton H (2005) Characterization and structural analysis of an active particulate methane monooxygenase trimer from Methylococcus capsulatus (Bath). Biochemistry 44:10954–10965
Lawton TJ, Rosenzweig AC (2016) Methane-oxidizing enzymes: an upstream problem in biological gas-to-liquids conversion. J Am Chem Soc 138:9327–9340
Leahy JG, Batchelor PJ, Morcomb SM (2003) Evolution of the soluble diiron monooxygenases. FEMS Microbiol Rev 27:449–479
Lee SJ (2016) Hydroxylation of methane through component interactions in soluble methane monooxygenases. J Microbiol 54:277–282
Lee SW, Keeney DR, Lim DH, Dispirito AA, Semrau JD (2006) Mixed pollutant degradation by Methylosinus trichosporium OB3b expressing either soluble or particulate methane monooxygenase: can the tortoise beat the hare? Appl Environ Microbiol 72:7503–7509
Lee SJ, McCormick MS, Lippard SJ, Cho US (2013) Control of substrate access to the active site in methane monooxygenase. Nature 494:380–384
Lieberman RL, Rosenzweig AC (2005) Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane. Nature 434:177–182
Lock M, Nichol T, Murrell JC, Smith TJ (2017) Mutagenesis and expression of methane monooxygenase to alter regioselectivity with aromatic substrates. FEMS Microbiol Lett 364. https://doi.org/10.1093/femsle/fnx137
Lontoh S, DiSpirito AA, Krema CL, Whittaker MR, Hooper AB, Semrau JD (2008) Differential inhibition in vivo of ammonia monooxygenase, soluble methane monooxygenase and membrane-associated methane monooxygenase by phenylacetylene. Env Microbiol 2:485–494
Martinho M, Choi DW, DiSpirito AA, Antholine WE, Semrau JD, Münck E (2007) Mössbauer studies of the membrane-associated methane monooxygenase from Methylococcus capsulatus Bath: evidence for a diiron center. J Am Chem Soc 129:15783–15785
McDonald IR, Bodrossy L, Chen Y, Murrell JC (2008) Molecular ecology techniques for the study of aerobic methanotrophs. Appl Environ Microbiol 74:1305–1315
Murrell JC, McDonald IR, Gilbert B (2000) Regulation of expression of methane monooxygenases by copper ions. Trends Microbiol 8:221–225
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
Nguyen HT, Elliott SJ, Yip JH, Chan SI (1998) The particulate methane monooxygenase from Methylococcus capsulatus (Bath) is a novel copper-containing three-subunit enzyme. J Biol Chem 273:7957–7978
Nichol T, Murrell JC, Smith TJ (2015) Controlling the activities of the diiron centre in bacterial monooxygenases: lessons from mutagenesis and biodiversity. Eur J Inorg Chem 2015: 3419–3431
Pieja AJ, Morse MC, Cal AJ (2017) Methane to bioproducts: the future of the bioeconomy? Curr Opin Chem Biol 41:123–131
Richards AO, Stanley SH, Suzuki M, Dalton H (1994) The biotransformation of propylene to propylene oxide by Methylococcus capsulatus (Bath). Biocatalysis 8:253–267
Ricke P, Erkel C, Kube M, Reinhardt R, Liesack W (2004) Comparative analysis of the conventional and novel pmo (particulate methane monooxygenase) operons from Methylocystis strain SC2. Appl Environ Microbiol 70:3055–3063
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
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 29:141–152
Ross MO, Rosenzweig AC (2017) A tale of two methane monooxygenases. J Biol Inorg Chem 22:307–319
Sazinsky MH, Lippard SJ (2015) Methane monooxygenase: functionalizing methane at iron and copper. In: Kroneck PMH, Sosa Torres ME (eds) Sustaining life on planet earth: Metalloenzymes mastering dioxygen and other chewy gases. Springer, Heidelberg, pp 205–256
Semrau JD, DiSpirito AA, Yoon S (2010) Methanotrophs and copper. FEMS Microbiol Rev 34:496–531
Semrau JD, Jagadevan S, DiSpirito AA, Khalifa A, Scanlan J, Bergman BH, Freemeier BC, Baral BS, Bandow NL, Vorobev A, Haft DH, Vuilleumier S, Murrell JC (2013) Methanobactin and MmoD work in concert to act as the ‘copper-switch’in methanotrophs. Environ Microbiol 15:3077–3086
Semrau JD, DiSpirito AA, Gu W, Yoon S (2018) Metals and Methanotrophy. Appl Environ Microbiol 84:AEM-02289
Sigdel S, Hui G, Smith TJ, Murrell JC, Lee JK (2015) Molecular dynamics simulation to rationalize regioselective hydroxylation of aromatic substrates by soluble methane monooxygenase. Bioorg Med Chem Lett 25:1611–1615
Sirajuddin S, Rosenzweig AC (2015) Enzymatic oxidation of methane. Biochemistry 54:2283–2294.
Smith DDS, Dalton H (1989) Solubilization of methane monooxygenase from Methylococcus capsulatus (Bath). Eur J Biochem 182:667–671
Smith TJ, Dalton H (2004) Biocatalysis by methane monooxygenase and its implications for the petroleum industry. Petroleum biotechnology: developments and perspectives. Stud Surf Sci Catal 151:177–192
Smith TJ, Murrell JC (2008) Methanotrophs. In: Flickinger M (ed) Encyclopedia of industrial biotechnology. Wiley, Hoboken, NJ
Smith TJ, Slade SE, Burton NP, Murrell JC, Dalton H (2002) An improved system for protein engineering of the hydroxylase component of soluble methane monooxygenase. Appl Environ Microbiol 68:5265–5273
Stafford GP, Scanlan J, McDonald IR, Murrell JC (2003) Characterization of rpoN, mmoR and mmoG, genes involved in regulating the expression of soluble methane monooxygenase in Methylosinus trichosporium OB3b. Microbiology 149:1771–1784
Stanley SH, Prior SD, Leak DJ, Dalton H (1983) Copper stress underlies the fundamental change in intracellular location of methane monooxygenase in methane-oxidizing organisms: studies in batch and continuous cultures. Biotechnol Lett 5:487–492
Stolyar S, Franke M, Lidstrom ME (2001) Expression of individual copies of Methylococcus capsulatus Bath particulate methane monooxygenase genes. J Bacteriol 183:1810–1812
Strong PJ, Xie S, Clarke WP (2015) Methane as a resource: can the methanotrophs add value? Environ Sci Technol 49:4001–4018
Tchawa Yimga M, Dunfield PF, Ricke P, Heyer J, Liesack W (2003) Wide distribution of a novel pmoA-like gene copy among type II methanotrophs, and its expression in Methylocystis strain SC2. Appl Environ Microbiol 69:5593
Theisen AR, Ali HM, Radajewski S, Dumont MG, Dunfield PF, McDonald IR, Dedysh SN, Miguez CB, Murrell JC (2005) Regulation of methane oxidation in the facultative methanotroph Methylocella silvestris BL2. Mol Microbiol 58:682–692
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
Trehoux A, Mahy JP, Avenier F (2016) A growing family of O2 activating dinuclear iron enzymes with key catalytic diiron (III)-peroxo intermediates: biological systems and chemical models. Coord Chem Rev 322:142–158
Trotsenko YA, Murrell JC (2008) Metabolic aspects of aerobic obligate methylotrophy. Adv App Microbiol 63:183–229
Vita N, Platsaki S, Baslé A, Allen SJ, Paterson NG, Crombie AT, Murrell JC, Waldron KJ, Dennison C (2015) A four-helix bundle stores copper for methane oxidation. Nature 525:140–143
Vita N, Landolfi G, Baslé A, Platsaki S, Lee J, Waldron KJ, Dennison C (2016) Bacterial cytosolic proteins with a high capacity for Cu (I) that protect against copper toxicity. Sci Rep 6:39065
Vorobev AV, Baani M, Doronina NV, Brady AL, Liesack W, Dunfield PF, Dedysh SN (2011) Methyloferula stellata gen. nov., sp. nov., an acidophilic, obligately methanotrophic bacterium that possesses only a soluble methane monooxygenase. Int J Syst Evol Microbiol 61:2456–2463
Walters KJ, Gassner GT, Lippard SJ, Wagner G (1999) Structure of the soluble methane monooxygenase regulatory protein B. Proc Natl Acad Sci USA 96:7877–7882
Welte KU, Rasigraf O, Vaksmaa A, Versantvoort W, Arshad A, Op den Camp HJM, Jetten MSM, Lüke C, Reimann J (2016) Environ Microbiol Rep 8:941–955
Yoon S, Im J, Bandow N, DiSpirito AA, Semrau JD (2011) Constitutive expression of pMMO by Methylocystis strain SB2 when grown on multi-carbon substrates: implications for biodegradation of chlorinated ethenes. Environ Microbiol Rep 3:182–188
Zahn JA, DiSpirito AA (1996) Membrane-associated methane monooxygenase from Methylococcus capsulatus (Bath). J Bacteriol 178:1018–1029
Zhang S, Karthikeyan R, Fernando SD (2017) Low-temperature biological activation of methane: structure, function and molecular interactions of soluble and particulate methane monooxygenases. Rev Environ Sci Biotechnol 6:611–623
Zheng H, Lipscomb JD (2006) Regulation of methane monooxygenase catalysis based on size exclusion and quantum tunneling. Biochemistry 45:1685–1692
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this entry
Cite this entry
Nichol, T., Murrell, J.C., Smith, T.J. (2019). Biochemistry and Molecular Biology of Methane Monooxygenase. In: Rojo, F. (eds) Aerobic Utilization of Hydrocarbons, Oils, and Lipids. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-50418-6_5
Download citation
DOI: https://doi.org/10.1007/978-3-319-50418-6_5
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-50417-9
Online ISBN: 978-3-319-50418-6
eBook Packages: Biomedical and Life SciencesReference Module Biomedical and Life Sciences