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Metals in Methanotrophy

  • Norma Cecilia Martinez-Gomez
  • Elizabeth Skovran
Chapter

Abstract

Metals play a pivotal role during one-carbon metabolism as they are important catalysts for numerous enzymatic reactions, can be used for electron transfer, enable radical chemistry, and enhance enzymatic substrate affinity. Metals also coordinate the expression of genes that are involved in their own sensing, sequestration, transport, storage, and use to ensure that their accumulation does not become toxic. Metals such as copper (Cu), iron (Fe), lanthanides (Ln), cobalt (Co), zinc (Zn), molybdenum (Mo), and tungsten (W) are particularly important for methanotrophy. This chapter will describe the role in catalysis for each one of these micronutrients along with the structural and mechanistic details of important catalytic centers. Sensing, uptake, and sequestration mechanisms will be highlighted along with changes in metabolism due to metal limitations during environmental and biotechnological processes. The diverse metal-dependent regulatory effects during methanotrophy will also be addressed, and metal-dependent advances in biotechnology and sustainability will be briefly described.

References

  1. Acheson JF, Bailey LJ, Elsen NL, Fox BG (2014) Structural basis for biomolecular recognition in overlapping binding sites in a diiron enzyme system. Nat Commun 5:5009CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anthony C (1986) Bacterial oxidation of methane and methanol. Adv Microb Physiol 27:113–210CrossRefPubMedGoogle Scholar
  3. Balasubramanian R, Smith SM, Rawat S, Yatsunyk LA, Stemmler TL, Rosenzweig AC (2010) Oxidation of methane by a biological dicopper centre. Nature 465:115–119CrossRefPubMedPubMedCentralGoogle Scholar
  4. Balasubramanian R, Rosenzweig AC (2007) Structural and mechanistic insights into methane oxidation by particulate methane monooxygenase. Acc Chem Res 40:573–580CrossRefPubMedGoogle Scholar
  5. 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 369:417–427CrossRefPubMedPubMedCentralGoogle Scholar
  6. Behling LA, Hartsel SC, Lewis DE, DiSpirito AA, Choi DW, Masterson LR, Veglia G, Gallagher WH (2008) NMR, mass spectrometry and chemical evidence reveal a different chemical structure for methanobactin that contains oxazolone rings. J Am Chem Soc 130:12604–12605CrossRefPubMedPubMedCentralGoogle Scholar
  7. Blanksby SJ, Ellison GB (2003) Bond dissociation energies of organic molecules. Acc Chem Res 36:255–263CrossRefPubMedGoogle Scholar
  8. Bogart JA, Lewis AJ, Schelter EJ (2015) DFT study of the active site of the XoxF-type natural, cerium-dependent methanol dehydrogenase enzyme. Chemistry 21:1743–1748CrossRefPubMedGoogle Scholar
  9. Chatwood LL, Müller J, Gross JD, Wagner G, Lippard SJ (2004) NMR structure of the flavin domain from soluble methane monooxygenase reductase from Methylococcus capsulatus (Bath). Biochemistry 43:11983–11991CrossRefPubMedGoogle Scholar
  10. Chistoserdova L (2011) Modularity of methylotrophy, revisited. Environ Microbiol 13:2603–26022CrossRefPubMedGoogle Scholar
  11. Choi DW, Kunz RC, Boyd ES et al (2003) The membrane-associated methane monooxygenase (pMMO) and pMMO-NADH: quinone oxidoreductase complex from Methylococcus capsulatus Bath. J Bacteriol 185:5755–5764CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chou HH, Berthet J, Marx CJ (2009) Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation. PLoS Genetics 5:e1000652CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chu F, Beck DA, Lidstrom ME (2016) MxaY regulates the lanthanide-mediated methanol dehydrogenase switch in Methylomicrobium buryatense. Peer J 4:e2435CrossRefPubMedGoogle Scholar
  14. Chu F, Lidstrom ME (2016) XoxF acts as the predominant methanol dehydrogenase in the Type I methanotroph Methylomicrobium buryatense. J Bacteriol 198:1317–1325CrossRefPubMedPubMedCentralGoogle Scholar
  15. Colby J, Dalton H (1979) Characterization of the second prosthetic group of the flavoenzyme NADH-acceptor reductase (component C) of the methane monooxygenase of Methylococcus capsulatus (Bath). Biochem J 177:903–908CrossRefPubMedPubMedCentralGoogle Scholar
  16. Cook SA, Shiemke AK (2002) Evidence that a type-2 NADH:quinone oxidoreductase mediates electron transfer to particulate methane monooxygenase in Methylococcus capsulatus. Arch Biochem Biophys 398:32−40CrossRefPubMedGoogle Scholar
  17. Csaki R, Bodrossy L, Klem J, Murrell JC, Kovacs K (2003) Genes involved in the copper-dependent regulation of soluble methane monooxygenase of Methylococcus capsulatus (Bath):cloning, sequencing and mutational analysis. Microbiology 149:1785–1795CrossRefPubMedGoogle Scholar
  18. Culpepper MA, Rosenzweig AC (2014) Structure and protein-protein interactions of methanol dehydrogenase from Methylococcus capsulatus (Bath). Biochemistry 53:6211–6219CrossRefPubMedPubMedCentralGoogle Scholar
  19. Culpepper MA, Cutsail GE III, Gunderson WA, Hoffman BM, Rosenzweig AC (2014) Identification of the valence and coordination environment of the particulate methane monooxygenase copper centers by advanced EPR characterization. J Am Chem Soc 136:11767–11775CrossRefPubMedPubMedCentralGoogle Scholar
  20. Dassama LMK, Kenney GE, Ro SY, Zielazinski EL, Rosenzweig AC (2016) Methanobactin transport machinery. PNAS 113:13027–13032CrossRefPubMedGoogle Scholar
  21. Davidson VL (2004) Electron transfer in quinoproteins. Arch Biochem Biophys 428:32–40CrossRefPubMedGoogle Scholar
  22. Delaney NF, Kaczmarek ME, Ward LM, Swanson PK, Lee MC, Marx CJ (2013) Development of an optimized medium, strain and high-throughput culturing methods for Methylobacterium extorquens. PLoS One 8:e62957CrossRefPubMedPubMedCentralGoogle Scholar
  23. Dennison C, Vijgenboom E, de Vries S, van der Oost J, Canters GW (1995) Introduction of a CuA site into the blue copper protein amicyanin from Thiobacillus versutus. FEBS Lett 365:92–94CrossRefPubMedGoogle Scholar
  24. 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 80:387–409CrossRefPubMedPubMedCentralGoogle Scholar
  25. Erb TJ, Berg IA, Brecht V, Müller M, Fuchs G, Alber BE (2007) Synthesis of C5-dicarboxylic acids from C2-units involving crotonyl-CoA carboxylase/reductase: the ethylmalonyl-CoA pathway. Proc Natl Acad Sci USA 104:10631–10636CrossRefPubMedGoogle Scholar
  26. Farhan Ul Haque M, Kalidass B, Bandow N, Turpin EA, DiSpirito AA, Semrau JD (2015) Cerium regulates expression of alternative methanol dehydrogenases in Methylosinus trichosporium OB3b. Appl Environ Microbiol 81:217546–217552Google Scholar
  27. 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 266:540–550PubMedPubMedCentralGoogle Scholar
  28. 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 264:10023–10033PubMedGoogle Scholar
  29. Fu Y, Beck DA, Lidstrom ME (2016) Difference in C3–C4 metabolism underlies tradeoff between growth rate and biomass yield in Methylobacterium extorquens AM1. BMC Microbiol 16:156CrossRefPubMedPubMedCentralGoogle Scholar
  30. Glass JB, Orphan VJ (2012) Trace metal requirements for microbial enzymes involved in the production and consumption of methane and nitrous oxide. Front Microbiol 3:61PubMedPubMedCentralGoogle Scholar
  31. Good NM, Vu HN, Suriano CJ, Subuyuj GA, Skovran E, Martinez-Gomez NC (2016) Pyrroloquinoline quinone ethanol dehydrogenase in Methylobacterium extorquens AM1 extends lanthanide-dependent metabolism to multicarbon substrates. J Bacteriol 198:3109–3118CrossRefPubMedPubMedCentralGoogle Scholar
  32. Gu W, Farhan Ul Haque M, DiSpirito AA, Semrau JD (2016b) Uptake and effect of rare earth elements on gene expression in Methylosinus trichosporium OB3b. FEMS Microbiol Lett 363.  https://doi.org/10.1093/femsle/fnw129
  33. Gu W, Farhan Ul Haque M, Baral BS, Turpin EA, Bandow NL, Kremmer E, Flatley A, Zischka H, DiSpirito AA, Semrau JD (2016a) A TonB-dependent transporter is responsible for Methanobactin Uptake by Methylosinus trichosporium OB3b. Appl Environ Microbiol 82:1917–1923CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 47:6793–6801CrossRefPubMedPubMedCentralGoogle Scholar
  35. Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60:439–471PubMedPubMedCentralGoogle Scholar
  36. Helland R, Fjellbirkeland A, Karlsen OA, Ve T, Lillehaug JR, Jensen HB (2008) An oxidized tryptophan facilitates copper binding in Methylococcus capsulatus-secreted protein MopE. J Biol Chem 283:13897–13904CrossRefPubMedGoogle Scholar
  37. Hibi Y, Asai K, Arafuka H, Hamajima M, Iwama T, Kawai K (2011) Molecular structure of La3+-induced methanol dehydrogenase-like protein in Methylobacterium radiotolerans. J Biosci Bioeng 111:547–549CrossRefPubMedGoogle Scholar
  38. Hu B, Lidstrom ME (2014) Metabolic engineering of Methylobacterium extorquens AM1 for 1-butanol production. Biotechnol Biofuels 7:156CrossRefPubMedPubMedCentralGoogle Scholar
  39. Itoyama S, Doitomi K, Kamachi T, Shiota Y, Yoshizawa K (2016) Possible peroxo state of the dicopper site of particulate methane monooxygenase from combined quantum mechanics and molecular mechanics calculations. Inorg Chem 55:2771–2277CrossRefPubMedGoogle Scholar
  40. Karlsen OA, Berven FS, Stafford GP, Larsen Ø, Murrell JC, Jensen HB, Fjellbirkeland A (2003) The surface-associated and secreted MopE protein of Methylococcus capsulatus (Bath) responds to changes in the concentration of copper in the growth medium. Appl Environ Microbiol 69:2386–2388CrossRefPubMedPubMedCentralGoogle Scholar
  41. Keltjens JT, Pol A, Reimann J, Op den Camp HJ (2014) PQQ-dependent methanol dehydrogenases: rare-earth elements make a difference. Appl Microbiol Biotechnol 98:6163–6183CrossRefPubMedGoogle Scholar
  42. Kenney GE, Goering AW, Ross MO, Dehart CJ, Thomas PM, Hoffman BM, Rosenzweig AC (2016) Characterization of Methanobactin from Methylosinus sp. LW4. J Am Chem Soc 138:11124–11127CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kenney GE, Rosenzweig AC (2013) Genome mining for methanobactins. BMC Biol 11:17CrossRefPubMedPubMedCentralGoogle Scholar
  44. Kiefer P, Buchhaupt M, Christen P, Kaup B, Schrader J, Vorholt JA (2009) Metabolite profiling uncovers plasmid-induced cobalt limitation under methylotrophic growth conditions. PLoS One 4:e7831CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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 44:5140–5148CrossRefPubMedGoogle Scholar
  46. Kim HJ, Graham DW, DiSpirito AA, Alterman MA, Galeva N, Larive CK, Asunskis D, Sherwood PM (2004) Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria. Science 305:1612–1615CrossRefPubMedGoogle Scholar
  47. Lankford CE, Byers BR (1973) Bacterial assimilation of iron. Crit Rev Microbiol 2:273–331CrossRefGoogle Scholar
  48. Larsen Ø, Karlsen OA (2016) Transcriptomic profiling of Methylococcus capsulatus (Bath) during growth with two different methane monooxygenases. Microbiologyopen 5:254–267CrossRefPubMedGoogle Scholar
  49. Lawton TJ, Rosenzweig AC (2016) Methane-oxidizing enzymes: an upstream problem in biological gas-to-liquids conversion. J AM Chem Soc 138:9327–9340CrossRefPubMedPubMedCentralGoogle Scholar
  50. Leak DJ, Dalton H (1986) Growth yields of methanotrophs. A theoretical analysis. Appl Microbiol Biotechnol 23:477–481CrossRefGoogle Scholar
  51. Lee SJ, McCormick MS, Lippard SJ, Cho U-S (2013) Control of substrate access to the active site in methane monooxygenase. Nature 494:380–384CrossRefPubMedPubMedCentralGoogle Scholar
  52. 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 72:7503–750910CrossRefPubMedPubMedCentralGoogle Scholar
  53. Lee SY, Park HS, Lee Y, Lee SH (2002) Production of chiral and other valuable compounds from microbial polyesters. In: Doi Y, Steinbüchel A (eds) Biopolymers, polyesters, vol 3. Wiley-VCH, Weinheim, pp 375–387Google Scholar
  54. Leopoldini M, Russo N, Toscano M (2007) The preferred reaction path for the oxidation of methanol by PQQ containing methanol dehydrogenase: addition–elimination versus hydride-transfer mechanism. Chem Eur 13:2109–2117CrossRefGoogle Scholar
  55. Lieberman RL, Rosenzweig AC (2005) Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane. Nature 434:177–182CrossRefPubMedGoogle Scholar
  56. Lim CS, Kampf JW, Pecoraro VL (2009) Establishing the binding affinity of organic carboxylates to 15-metallacrown-5 complexes. Inorg Chem 48:5224–5233CrossRefPubMedGoogle Scholar
  57. Lipscomb JD (1994) Biochemistry of the soluble methane monooxygenase. Annu Rev Microbiol 48:371–399CrossRefPubMedGoogle Scholar
  58. Liu Y, Nesheim JC, Lee SK, Lipscomb JD (1995) Gating effects of component B on oxygen activation by the methane monooxygenase hydroxylase component. J Biol Chem 270:24662–24665CrossRefPubMedGoogle Scholar
  59. Maia LB, Moura JJG, Moura I (2015) Molybdenum and tungsten-dependent formate dehydrogenases. J Biol Inorg 20:287–309CrossRefGoogle Scholar
  60. Martinez-Gomez NC, Vu HN, Skovran E (2016) Lanthanide chemistry: from coordination in chemical complexes shaping our technology to coordination in enzymes shaping bacterial metabolism. Inorg Chem 55:10083–10089CrossRefPubMedGoogle Scholar
  61. 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 129:15783–15785CrossRefPubMedPubMedCentralGoogle Scholar
  62. Matsen JB, Yang S, Stein LY, Beck D, Kalyuzhnaya MG (2013) Global molecular analyses of methane metabolism in Methanotrophic Alphaproteobacterium, Methylosinus trichosporium OB3b. Part I: Transcriptomic study. Front Microbiol 4:40CrossRefPubMedPubMedCentralGoogle Scholar
  63. Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413–451CrossRefPubMedPubMedCentralGoogle Scholar
  64. Morton JD, Hayes KF, Semrau JD (2000) Bioavailability of chelated and soil-adsorbed copper to Methylosinus trichosporium OB3b. Environ Sci Technol 34:4917–4922CrossRefGoogle Scholar
  65. Müller 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 41:42–51CrossRefPubMedGoogle Scholar
  66. Murrell JC, McDonald IR, Gilbert B (2000) Regulation of expression of methane monooxygenases by copper ions. Trends Microbiol 8:221–225CrossRefPubMedGoogle Scholar
  67. 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 45:11905–11914CrossRefPubMedGoogle Scholar
  68. Nakagawa T, Mitsui R, Tani A, Sasa K, Tashiro S, Iwama T, Hayakawa T, Kawai K (2012) A catalytic role of XoxF1 as La3+-dependent methanol dehydrogenase in Methylobacterium extorquens strain AM1. PLoS One 7:e50480CrossRefPubMedPubMedCentralGoogle Scholar
  69. Nielsen AK, Gerdes K, Murrell JC (1997) Copper-dependent reciprocal transcriptional regulation of methane monooxygenase genes in Methylococcus capsulatus and Methylosinus trichosporium. Mol Microbiol 25:399–409CrossRefPubMedGoogle Scholar
  70. Prejanò M, Marino T, Russo N (2017) How can work methanol dehydrogenase from Methylacidiphilum fumariolicum with the alien Ce(III) ion in the active center? A theoretical study. Chemistry 23:8652–8657CrossRefPubMedGoogle Scholar
  71. Pol A, Barends TR, Dietl A, Khadem AF, Eygensteyn J, Jetten MS, Op den Camp HJ (2014) Rare earth metals are essential for methanotrophic life in volcanic mudpots. Environ Microbiol 16:255–264CrossRefPubMedGoogle Scholar
  72. Richardson DJ, Edwards MJ, White GF, Baiden N, Hartshorne RS, Fredrickson JK et al (2012) Exploring the biochemistry at the extracellular redox frontier of bacterial mineral Fe (III) respiration. Biochem Soc Trans 40:493–500CrossRefPubMedGoogle Scholar
  73. 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. Protein Struct Funct Genet 29:141–152CrossRefGoogle Scholar
  74. Sazinsky MH, Lippard SJ (2015) Methane monooxygenase: functionalizing methane at iron and copper. Met Ions Life Sci 15:205–256PubMedGoogle Scholar
  75. Schmidt S, Christen P, Kiefer P, Vorholt JA (2010) Functional investigation of methanol dehydrogenase-like protein XoxF in Methylobacterium extorquens AM1. Microbiology 156:2575–2586CrossRefPubMedGoogle Scholar
  76. 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 15:3077–3086PubMedGoogle Scholar
  77. Semrau JD (2011) Bioremediation via methanotrophy: overview of recent findings and suggestions for future research. Front Microbiol 2:209CrossRefPubMedPubMedCentralGoogle Scholar
  78. Semrau JD, DiSpirito AA, Yoon S (2010) Methanotrophs and copper. FEMS 34:496–531Google Scholar
  79. Shiemke AK, Arp DJ, Sayavedra-Soto LA (2004) Inhibition of membrane-bound methane monooxygenase and ammonia monooxygenase by diphenyliodonium: implications for electron transfer. J Bacteriol 186:928–937CrossRefPubMedPubMedCentralGoogle Scholar
  80. Shiota Y, Juhász G, Yoshizawa K (2013) Role of tyrosine residue in methane activation at the dicopper site of particulate methane monooxygenase: a density functional theory study. Inorg Chem 52:7907–7917CrossRefPubMedGoogle Scholar
  81. Shiota Y, Yoshizawa K (2009) Comparison of the reactivity of bis(mu-oxo)CuIICuIII and CuIIICuIII species to methane. Inorg Chem 48:838–845CrossRefPubMedGoogle Scholar
  82. Sirajuddin S, Rosenzweig AC (2015) Enzymatic oxidation of methane. Biochemistry 54:2283–2294CrossRefPubMedPubMedCentralGoogle Scholar
  83. Sonntag F, Buchhaupt M, Schrader J (2014) Thioesterases for ethylmalonyl-CoA pathway derived dicarboxylic acid production in Methylobacterium extorquens AM1. Appl Microbiol Biotechnol 98:4533–4544CrossRefPubMedGoogle Scholar
  84. Stafford GP, Scanlan J, McDonald IR, Murrell JC (2003) rpoN, mmoR and mmoG, genes involved in the expression of soluble methane monooxygenase in Methylosinus trichosporium OB3b. Microbiology 149:1771–1784CrossRefPubMedGoogle Scholar
  85. Tonge GM, Harrison DEF, Knowles CJ, Higgins IJ (1975) Properties and partial purification of the methane-oxidizing enzyme system from Methylosinus trichosporium. FEBS Lett 58:293–299CrossRefPubMedGoogle Scholar
  86. Vorobev A, Beck DA, Kalyuzhnaya MG, Lidstrom ME, Chistoserdova L (2013) Comparative transcriptomics in three Methylophilaceae species uncover different strategies for environmental adaptation. Peer J 1:e115CrossRefPubMedGoogle Scholar
  87. Vu HN, Subuyuj GA, Vijayakumar S, Good NM, Martinez-Gomez NC, Skovran E (2016) Lanthanide-dependent regulation of methanol oxidation systems in Methylobacterium extorquens AM1 and their contribution to methanol growth. J Bacteriol 198:1250–1259CrossRefPubMedPubMedCentralGoogle Scholar
  88. Wang W, Liang AD, Lippard SJ (2015) Coupling oxygen consumption with hydrocarbon oxidation in bacterial multicomponent monooxygenases. Acc Chem Res 48:2632–2639CrossRefPubMedPubMedCentralGoogle Scholar
  89. Wang W, 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 136:2244–2247CrossRefPubMedPubMedCentralGoogle Scholar
  90. Watkins JD, Bocarsly AB (2014) Direct reduction of carbon dioxide to formate in high-gas-capacity ionic liquids at post-transition-metal electrodes. ChemSusChem 7:284–290CrossRefPubMedGoogle Scholar
  91. Werpy T, Petersen G (2004) Top value added chemicals from biomass: Volume I. Results of screening for potential candidates from sugars and synthesis gas other information Medium: ED; Size: 76 ppGoogle Scholar
  92. Yoon S, DiSpirito AA, Kraemer SM, Semarau JD (2010) A simple assay for screening microorganisms for Chalkophore production. Environ Microbiol Rep 2:295–303CrossRefPubMedGoogle Scholar
  93. Yoshizawa K, Shiota Y (2006) Conversion of methane to methanol at the mononuclear and dinuclear copper sites of Particulate Methane Monooxygenase (pMMO): a DFT and QM/MM study. J Am Chem Soc 128:9873–9881CrossRefPubMedGoogle Scholar
  94. Zahn JA, DiSpirito AA (1996) Membrane-associated methane monooxygenase from Methylococcus capsulatus (Bath). J Bacteriol 178:1018–1029CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Norma Cecilia Martinez-Gomez
    • 1
  • Elizabeth Skovran
    • 2
  1. 1.Michigan State UniversityEast LansingUSA
  2. 2.San Jose State UniversitySan JoseUSA

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