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Metabolic Engineering of Methanotrophic Bacteria for Industrial Biomanufacturing

  • Calvin A. Henard
  • Michael T. Guarnieri
Chapter

Abstract

CH4 offers a promising, high-volume petroleum replacement for fuel and chemical bioprocesses. Recent advances in gas recovery technologies have facilitated access to previously inaccessible natural gas reserves, while biogas generated from anaerobic digestion of waste streams offers a versatile, renewable CH4 source. Importantly, CH4 is also the second most abundant greenhouse gas (GHG), with nearly 60% of emissions derived from anthropogenic sources. However, the gaseous state of CH4 makes for a lack of compatibility with current transportation and industrial manufacturing infrastructure, limiting its utilization as a transportation fuel and intermediate in biochemical processes. Resurgent interest in CH4 upgrading has pushed microbial conversion of CH4 to fuels and value-added chemicals to the forefront of industrial bioprocessing. CH4 bioconversion offers both CH4 valorization and GHG emission reduction potential and importantly offers a scalable, modular, and selective approach to CH4 utilization compared to conventional physical and chemical conversion strategies. However, as noted above, advances in CH4 biocatalysis have been constrained by limited genetic tractability of natural CH4-consuming microbes. In this chapter, we review recent advances in methanotrophic genetic and genomic tool development and metabolic engineering.

References

  1. Akberdin IR, Thompson M, Hamilton R, Desai N, Alexander D, Henard CA, Guarnieri MT, Kalyuzhnaya MG (2018) Methane utilization in Methylomicrobium alcaliphilum 20ZR: a systems approach. Sci Rep 8(1):2512CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anthony C, Williams P (2003) The structure and mechanism of methanol dehydrogenase. Biochim Biophys Acta 1647:18–23.  https://doi.org/10.1016/S1570-9639(03)00042-6CrossRefPubMedGoogle Scholar
  3. Baani M, Liesack W (2008) Two isozymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp. strain SC2. Proc Natl Acad Sci USA 105:10203–10208.  https://doi.org/10.1073/pnas.0702643105CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baxter NJ, Hirt RP, Bodrossy L et al (2002) The ribulose-1,5-bisphosphate carboxylase/oxygenase gene cluster of Methylococcus capsulatus (Bath). Arch Microbiol 177:279–289.  https://doi.org/10.1007/s00203-001-0387-xCrossRefPubMedGoogle Scholar
  5. Boden R, Cunliffe M, Scanlan J et al (2011) Complete genome sequence of the aerobic marine methanotroph Methylomonas methanica MC09. J Bacteriol 193:7001–7002.  https://doi.org/10.1128/JB.06267-11CrossRefPubMedPubMedCentralGoogle Scholar
  6. Clomburg JM, Crumbley AM, Gonzalez R (2017) Industrial biomanufacturing: the future of chemical production. Science 355:aag0804.  https://doi.org/10.1126/science.aag0804CrossRefPubMedGoogle Scholar
  7. Conrado RJ, Gonzalez R (2014) Chemistry. Envisioning the bioconversion of methane to liquid fuels. Science 343:621–623.  https://doi.org/10.1126/science.1246929CrossRefPubMedGoogle Scholar
  8. Crombie A, Murrell JC (2011) Development of a system for genetic manipulation of the facultative methanotroph Methylocella silvestris BL2. Methods Enzymol 495:119–133.  https://doi.org/10.1016/B978-0-12-386905-0.00008-5CrossRefPubMedGoogle Scholar
  9. Culpepper MA, Rosenzweig AC (2014) Structure and protein-protein interactions of methanol dehydrogenase from Methylococcus capsulatus (Bath). Biochemistry 53:6211–6219.  https://doi.org/10.1021/bi500850jCrossRefPubMedPubMedCentralGoogle Scholar
  10. Fei Q, Guarnieri MT, Tao L et al (2014) Bioconversion of natural gas to liquid fuel: opportunities and challenges. Biotechnol Adv 32:596–614.  https://doi.org/10.1016/j.biotechadv.2014.03.011CrossRefPubMedGoogle Scholar
  11. Flynn JD, Hirayama H, Sakai Y et al (2016) Draft genome sequences of gammaproteobacterial methanotrophs isolated from marine ecosystems. Genome Announc 4:e01629–e01615.  https://doi.org/10.1128/genomeA.01629-15CrossRefPubMedPubMedCentralGoogle Scholar
  12. Garst AD, Bassalo MC, Pines G et al (2017) Genome-wide mapping of mutations at single-nucleotide resolution for protein, metabolic and genome engineering. Nat Biotechnol 35:48–55.  https://doi.org/10.1038/nbt.3718CrossRefPubMedGoogle Scholar
  13. Gilman A, Laurens LM, Puri AW et al (2015) Bioreactor performance parameters for an industrially-promising methanotroph Methylomicrobium buryatense 5GB1. Microb Cell Fact 14:1–8.  https://doi.org/10.1186/s12934-015-0372-8CrossRefGoogle Scholar
  14. Hamilton R, Kits KD, Ramonovskaya VA et al (2015) Draft genomes of gammaproteobacterial methanotrophs isolated from terrestrial ecosystems. Genome Announc 3(3).  https://doi.org/10.1128/genomeA.00515-15
  15. Harwood JH, Williams E, Bainbridge BW (1972) Mutation of the methane oxidizing bacterium, Methylococcus capsulatus. J Appl Microbiol 35:99–108.  https://doi.org/10.1111/j.1365-2672.1972.tb03678.xCrossRefGoogle Scholar
  16. Haynes CA, Gonzalez R (2014) Rethinking biological activation of methane and conversion to liquid fuels. Nat Chem Biol 10:331–339.  https://doi.org/10.1038/nchembio.1509CrossRefPubMedGoogle Scholar
  17. Henard CA, Freed EF, Guarnieri MT (2015) Phosphoketolase pathway engineering for carbon-efficient biocatalysis. Curr Opin Biotechnol 36:183–188.  https://doi.org/10.1016/j.copbio.2015.08.018CrossRefPubMedGoogle Scholar
  18. Henard CA, Smith H, Dowe N et al (2016) Bioconversion of methane to lactate by an obligate methanotrophic bacterium. Sci Rep 6:1–9.  https://doi.org/10.1038/srep21585CrossRefGoogle Scholar
  19. Henard CA, Smith HK, Guarnieri MT (2017) Phosphoketolase overexpression increases biomass and lipid yield from methane in an obligate methanotrophic biocatalyst. Metab Eng 41:152–158CrossRefPubMedGoogle Scholar
  20. Kalyuzhanaya MG, Yang S, Matsen JB et al (2013) Global molecular analyses of methane metabolism in Methanotrophic alphaproteobacterium, Methylosinus trichosporium OB3b. Part II. Metabolomics and 13C-labeling study. Front Microbiol.  https://doi.org/10.3389/fmicb.2013.00070
  21. Kalyuzhnaya MG (2013) Global molecular analyses of methane metabolism in methanotrophic Alphaproteobacterium, Methylosinus trichosporium OB3b. Part II. metabolomics and 13C-labeling study. Front Microbiol:1–13.  https://doi.org/10.3389/fmicb.2013.00070/abstract
  22. Kalyuzhnaya MG, Yang S, Rozova ON et al (2013) Highly efficient methane biocatalysis revealed in a methanotrophic bacterium. Nat Commun 4.  https://doi.org/10.1038/ncomms3785
  23. Kalyuzhnaya MG, Puri AW, Lidstrom ME (2015) Metabolic engineering in methanotrophic bacteria. Metabolic Engineering 29:142–152.  https://doi.org/10.1016/j.ymben.2015.03.010CrossRefPubMedGoogle Scholar
  24. Khadem AF, Pol A, Wieczorek A et al (2011) Autotrophic methanotrophy in verrucomicrobia: Methylacidiphilum fumariolicumSolV uses the Calvin-Benson-Bassham cycle for carbon dioxide fixation. J Bacteriol 193:4438–4446.  https://doi.org/10.1128/JB.00407-11CrossRefPubMedPubMedCentralGoogle Scholar
  25. Khmelenina VN, Beck DAC, Munk C et al (2013) Draft genome sequence of Methylomicrobium buryatense Strain 5G, a Haloalkaline-Tolerant Methanotrophic Bacterium. Genome Announc 1(4).  https://doi.org/10.1128/genomeA.00053-13CrossRefGoogle Scholar
  26. Komor AC, Badran AH, Liu DR (2017) CRISPR-based technologies for the manipulation of eukaryotic genomes. Cell 168:20–36.  https://doi.org/10.1016/j.cell.2016.10.044CrossRefPubMedGoogle Scholar
  27. la Torre de A, Metivier A, Chu F et al (2015) Genome-scale metabolic reconstructions and theoretical investigation of methane conversion in Methylomicrobium buryatense strain 5G(B1). Microb Cell Fact 14:188.  https://doi.org/10.1186/s12934-015-0377-3CrossRefGoogle Scholar
  28. Larsen Ø, Karlsen OA (2016) Transcriptomic profiling of Methylococcus capsulatus (Bath) during growth with two different methane monooxygenases. MicrobiologyOpen 5:254–267.  https://doi.org/10.1002/mbo3.324CrossRefPubMedGoogle Scholar
  29. Lawton TJ, Rosenzweig AC (2016) Methane-oxidizing enzymes: an upstream problem in biological gas-to-liquids conversion. J Am Chem Soc 138:9327–9340.  https://doi.org/10.1021/jacs.6b04568CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lee OK, Hur DH, Nguyen D (2016) Metabolic engineering of methanotrophs and its application to production of chemicals and biofuels from methane. Biofuels Bioprod Biorefin 10(6):848–863.  https://doi.org/10.1002/bbb.1678/pdfCrossRefGoogle Scholar
  31. Lidstrom ME, Wopat AE (1984) Plasmids in methanotrophic bacteria: isolation, characterization and DNA hybridization analysis. Arch Microbiol 140:27–33.  https://doi.org/10.1007/BF00409767CrossRefPubMedGoogle Scholar
  32. Lynch MD, Gill RT (2006) Broad host range vectors for stable genomic library construction. Biotechnol Bioeng 94:151–158.  https://doi.org/10.1002/bit.20836CrossRefPubMedGoogle Scholar
  33. Makarova KS, Wolf YI, Alkhnbashi OS et al (2015) An updated evolutionary classification of CRISPR–Cas systems. Nat Rev Microbiol 13:722–736.  https://doi.org/10.1038/nrmicro3569CrossRefPubMedPubMedCentralGoogle Scholar
  34. Malashenko YR, Pirog TP, Romanovskaya VA et al (2001) Search for methanotrophic producers of exopolysaccharides. Appl Biochem Microbiol 37:599–602.  https://doi.org/10.1023/A:1012307202011CrossRefGoogle Scholar
  35. Marraffini LA (2016) The CRISPR-Cas system of Streptococcus pyogenes: function and applications. In: Ferretti JJ, Stevens DL, Fischetti VA (eds) Streptococcus pyogenes: basic biology to clinical manifestations. University of Oklahoma Health Sciences Center, OklahomaGoogle Scholar
  36. Marx CJ (2008) Development of a broad-host-range sacB-based vector for unmarked allelic exchange. BMC Res Notes 1(1).  https://doi.org/10.1186/1756-0500-1-1CrossRefPubMedPubMedCentralGoogle Scholar
  37. Marx CJ, Lidstrom ME (2002) Broad-host-range cre-lox system for antibiotic marker recycling in gram-negative bacteria. Biotechniques 33(5):1062–1067PubMedGoogle Scholar
  38. Matsen JB, Yang S, Stein LY et al (2013) Global molecular analyses of methane metabolism in Methanotrophic alphaproteobacterium, Methylosinus trichosporium OB3b. Part I: Transcriptomic study. Front Microbiol.  https://doi.org/10.3389/fmicb.2013.00040
  39. McPheat WL, Mann NH, Dalton H (1987) Isolation of mutants of the obligate methanotroph Methylomonas albus defective in growth on methane. Arch Microbiol 148:40–43.  https://doi.org/10.1007/BF00429645CrossRefGoogle Scholar
  40. Mohanraju P, Makarova KS, Zetsche B et al (2016) Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems. Science 353:aad5147.  https://doi.org/10.1126/science.aad5147CrossRefPubMedGoogle Scholar
  41. Murrell JC (1992) Genetics and molecular biology of methanotrophs. FEMS Microbiol Rev 8:233–248.  https://doi.org/10.1111/j.1574-6968.1992.tb04990.xCrossRefPubMedGoogle Scholar
  42. Mustakhimov II, But SY, Reshetnikov AS et al (2016) Homo- and heterologous reporter proteins for evaluation of promoter activity in Methylomicrobium alcaliphilum 20Z. Appl Biochem Microbiol 52:263–268.  https://doi.org/10.1134/S0003683816030157CrossRefGoogle Scholar
  43. Nicolaidis AA, Sargent AW (1987) Isolation of methane monooxygenase-deficient mutants from Methylosinus trichosporium OB3b using dichloromethane. FEMS Microbiol Lett 41:47–52.  https://doi.org/10.1111/j.1574-6968.1987.tb02139.xCrossRefGoogle Scholar
  44. Ojala DS, Beck DAC, Kalyuzhnaya MG (2011) Genetic systems for moderately halo(alkali)philic bacteria of the genus Methylomicrobium. Methods Enzymol 495:99–118.  https://doi.org/10.1016/B978-0-12-386905-0.00007-3CrossRefPubMedGoogle Scholar
  45. Puri AW, Owen S, Chu F et al (2015) Genetic Tools for the Industrially Promising Methanotroph Methylomicrobium buryatense. Appl Environ Microbiol 81:1775–1781.  https://doi.org/10.1128/AEM.03795-14CrossRefPubMedPubMedCentralGoogle Scholar
  46. Puri AW, Schaefer AL, Fu Y et al (2016) Quorum sensing in a methane-oxidizing bacterium. J Bacteriol 199(5).  https://doi.org/10.1128/JB.00773-16Google Scholar
  47. Rasigraf O, Kool DM, Jetten MSM et al (2014) Autotrophic carbon dioxide fixation via the Calvin-Benson-Bassham cycle by the denitrifying methanotroph “Candidatus Methylomirabilis oxyfera”. Appl Environ Microbiol 80:2451–2460.  https://doi.org/10.1128/AEM.04199-13CrossRefPubMedPubMedCentralGoogle Scholar
  48. Rohr LM, Teuber M, Meile L (2002) Phosphoketolase, a neglected enzyme of microbial carbohydrate metabolism. Chimia 56:270–273CrossRefGoogle Scholar
  49. Rozova ON, Khmelenina VN, Gavletdinova JZ et al (2015) Acetate kinase-an enzyme of the postulated phosphoketolase pathway in Methylomicrobium alcaliphilum 20Z. Antonie Van Leeuwenhoek 108:965–974.  https://doi.org/10.1007/s10482-015-0549-5CrossRefPubMedGoogle Scholar
  50. Sánchez B, Zúñiga M, González-Candelas F (2010) Bacterial and eukaryotic phosphoketolases: phylogeny, distribution and evolution. J Mol Microbiol Biotechnol 18:37–51CrossRefPubMedGoogle Scholar
  51. Sharan SK, Thomason LC, Kuznetsov SG, Court DL (2009) Recombineering: a homologous recombination-based method of genetic engineering. Nat Protoc 4:206–223.  https://doi.org/10.1038/nprot.2008.227CrossRefPubMedPubMedCentralGoogle Scholar
  52. Sharpe PL, Dicosimo D, Bosak MD et al (2007) Use of transposon promoter-probe vectors in the metabolic engineering of the obligate methanotroph Methylomonas sp. strain 16a for enhanced C40 carotenoid synthesis. Appl Environ Microbiol 73:1721–1728.  https://doi.org/10.1128/AEM.01332-06CrossRefPubMedPubMedCentralGoogle Scholar
  53. Sirajuddin S, Rosenzweig AC (2015) Enzymatic oxidation of methane. Biochemistry 54:2283–2294.  https://doi.org/10.1021/acs.biochem.5b00198CrossRefPubMedPubMedCentralGoogle Scholar
  54. Strong PJ, Xie S, Clarke WP (2015) Methane as a resource: can the methanotrophs add value? Environ Sci Technol 49:4001–4018.  https://doi.org/10.1021/es504242nCrossRefPubMedGoogle Scholar
  55. Toukdarian AE, Lidstrom ME (1984) Molecular construction and characterization of nif mutants of the obligate methanotroph Methylosinus sp. strain 6. J Bacteriol 157:979–983PubMedPubMedCentralGoogle Scholar
  56. Ungerer J, Pakrasi HB (2016) Cpf1 is a versatile tool for CRISPR genome editing across diverse species of Cyanobacteria. Sci Rep:1–9.  https://doi.org/10.1038/srep39681
  57. Vorobev A, Jagadevan S, Jain S et al (2014) Genomic and transcriptomic analyses of the facultative methanotroph Methylocystis sp. strain SB2 grown on methane or ethanol. Appl Environ Microbiol 80:3044–3052.  https://doi.org/10.1128/AEM.00218-14CrossRefPubMedPubMedCentralGoogle Scholar
  58. Vuilleumier S, Khmelenina VN, Bringel F et al (2012) Genome sequence of the haloalkaliphilic methanotrophic bacterium Methylomicrobium alcaliphilum 20Z. J Bacteriol 194(2):551–552CrossRefPubMedPubMedCentralGoogle Scholar
  59. Wang HH, Isaacs FJ, Carr PA et al (2009) Programming cells by multiplex genome engineering and accelerated evolution. Nature 460:894–898.  https://doi.org/10.1038/nature08187CrossRefPubMedPubMedCentralGoogle Scholar
  60. Williams E (1977) Mutation in the obligate methylotrophs Methylococcus capsulatus and Methylomonas albus. FEMS Microbiol Lett 2:293–296CrossRefGoogle Scholar
  61. Williams E, Bainbridge BW (1976) Mutation, repair mechanisms and transformation in the methane-utilizing bacterium, Methylococcus capsulatus. Proceedings of international symposium on the genetics of industrial microorganismsGoogle Scholar
  62. Woolston BM, Edgar S, Stephanopoulos G (2013) Metabolic engineering: past and future. Annu Rev Chem Biomol Eng 4:259–288.  https://doi.org/10.1146/annurev-chembioeng-061312-103312CrossRefPubMedGoogle Scholar
  63. Yan X, Chu F, Puri AW et al (2016) Electroporation-based genetic manipulation in Type I Methanotrophs. Appl Environ Microbiol 82:2062–2069.  https://doi.org/10.1128/AEM.03724-15CrossRefPubMedPubMedCentralGoogle Scholar
  64. Zetsche B, Gootenberg JS, Abudayyeh OO et al (2015) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-CAS system. Cell 163:759–771.  https://doi.org/10.1016/j.cell.2015.09.038CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.National Bioenergy CenterNational Renewable Energy LaboratoryGoldenUSA

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