Abstract
Recent developments in experimental technologies have transformed traditional microbial physiology into a data-rich or -omics discipline. As a result, it has caused a renaissance of the mathematical analysis of biological systems and stimulated the development of systems biology workflows which aim to provide a holistic vision of all cellular functions through genomics, transcriptomics, proteomics, metabolomics, and fluxomic data. In silico modeling of metabolic systems has become a powerful tool, providing insight into the complex processes in cellular metabolism and their underlying regulatory mechanisms, as well as potentially improving the biotechnological design of microbial strains with desired properties. In this chapter, we provide an overview of the systems biology of methane utilization, as an example of one unique microbial function that has been dissected using - omics technologies. We discuss the most recent advances in large-scale investigation and computational representation of related metabolic networks as well as highlight some challenges for further developments in the field.
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References
Akberdin IR, Kazantsev FV, Ermak TV, Timonov VS, Khlebodarova TM, Likhoshvai VA (2013) In silico cell: challenges and perspectives. Math Biol Bioinform 8(1):295–315
Akberdin IR, Thompson M, Hamilton R, Desai N, Alexander D, Henard CA, Guarnieri MT, Kalyuzhnaya MG (2018) Methane utilization in Methylomicrobium alcaliphilum 20Z R: a systems approach. Sci Rep 8:2512
Akberdin IR, But S, Collins D, Kalyuzhnaya MG (n.d.) Methane utilization in Methylomicrobium alcaliphilum 20ZR: mutagenesis-based investigation and dynamic modeling of the initial steps of methane oxidation. BMC Syst Biol (unpublished data)
Alon U (2006) An introduction to systems biology: design principles of biological circuits. CRC Press, Boca Raton, FL
Anthony C (1982) Biochemistry of methylotrophs. Academic Press, London
Anvar SY, Frank J, Pol A, Schmitz A, Kraaijeveld K, den Dunnen JT, den Camp HJO (2014) The genomic landscape of the verrucomicrobial methanotroph Methylacidiphilum fumariolicum SolV. BMC Genom 15(1):914
Beck DA, Kalyuzhnaya MG, Malfatti S, Tringe SG, del Rio TG, Ivanova N et al (2013) A metagenomic insight into freshwater methane-utilizing communities and evidence for cooperation between the Methylococcaceae and the Methylophilaceae. PeerJ 1:e23
Bensimon A, Heck AJ, Aebersold R (2012) Mass spectrometry-based proteomics and network biology. Ann Rev Biochem 81:379–405
Berven FS, Karlsen OA, Straume AH, Flikka K, Murrell JC, Fjellbirkeland A et al (2006) Analysing the outer membrane subproteome of Methylococcus capsulatus (Bath) using proteomics and novel biocomputing tools. Arch Microbiol 184(6):362–377
Best DJ, Higgins IJ (1981) Methane-oxidizing activity and membrane morphology in a methanolgrown obligate methanotroph, Methylosinus trichosporium OB3b. Microbiology 125(1):73–84
Büchel F, Rodriguez N, Swainston N, Wrzodek C, Czauderna T, Keller R et al (2013) Path2Models: large-scale generation of computational models from biochemical pathway maps. BMC Syst Biol 7(1):116
But SY, Khmelenina VN, Reshetnikov AS, Mustakhimov II, Kalyuzhnaya MG, Trotsenko YA (2015) Sucrose metabolism in halotolerant methanotroph Methylomicrobium alcaliphilum 20Z. Arch Microbiol 197(3):471–480
Caspi R, Billington R, Ferrer L, Foerster H, Fulcher CA, Keseler IM et al (2016) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res 44(D1):D471–D480
Cavill R, Jennen D, Kleinjans J, Briedé JJ (2015) Transcriptomic and metabolomic data integration. Brief Bioinform 17:bbv090
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(8):969–979
Chistoserdova L (2011) Modularity of methylotrophy, revisited. Environ Microbiol 13(10):2603–2622
Chistoserdova L, Lidstrom ME (2013) Aerobic methylotrophic prokaryotes. In: DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin, pp 267–285
Chu F, Lidstrom ME (2016) XoxF acts as the predominant methanol dehydrogenase in the type I methanotroph Methylomicrobium buryatense. J Bacteriol 198(8):1317–1325
Covert MW, Schilling CH, Famili I, Edwards JS, Goryanin II, Selkov E, Palsson BO (2001) Metabolic modeling of microbial strains in silico. Trends Biochem Sci 26(3):179–186
Crombie AT, Murrell JC (2014) Trace-gas metabolic versatility of the facultative methanotroph Methylocella silvestris. Nature 510:148–151
Crowther GJ, Kosály G, Lidstrom ME (2008) Formate as the main branch point for methylotrophic metabolism in Methylobacterium extorquens AM1. J Bacteriol 190(14):5057–5062
Culpepper MA, Rosenzweig AC (2012) Architecture and active site of particulate methane monooxygenase. Crit Rev Biochem Mol Biol 47(6):483–492
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 104(25):10631–10636
Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MM et al (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464(7288):543
Fei Q, Guarnieri MT, Tao L, Laurens LM, Dowe N, Pienkos PT (2014) Bioconversion of natural gas to liquid fuel: opportunities and challenges. Biotechnol Adv 32(3):596–614
Fu Y, Li Y, Lidstrom M (2017) The oxidative TCA cycle operates during methanotrophic growth of the Type I methanotroph Methylomicrobium buryatense 5GB1. Metab Eng 42:43–51
Gourion B, Rossignol M, Vorholt JA (2006) A proteomic study of Methylobacterium extorquens reveals a response regulator essential for epiphytic growth. Proc Natl Acad Sci 103(35):13186–13191
Hakemian AS, Rosenzweig AC (2007) The biochemistry of methane oxidation. Annu Rev Biochem 76:223–241
Haque MFU, 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(21):7546–7552
Haque MFU, Gu W, DiSpirito AA, Semrau JD (2016) Marker exchange mutagenesis of mxaF, encoding the large subunit of the Mxa methanol dehydrogenase, in Methylosinus trichosporium OB3b. Appl Environ Microbiol 82(5):1549–1555
Henard CA, Smith HK, Guarnieri MT (2017) Phosphoketolase overexpression increases biomass and lipid yield from methane in an obligate methanotrophic biocatalyst. Metab Eng 41:152–158
Hübner K, Sahle S, Kummer U (2011) Applications and trends in systems biology in biochemistry. FEBS J 278(16):2767–2857
Kalyuzhnaya MG, Hristova KR, Lidstrom ME, Chistoserdova L (2008) Characterization of a novel methanol dehydrogenase in representatives of Burkholderiales: implications for environmental detection of methylotrophy and evidence for convergent evolution. J Bacteriol 190(11):3817–3823
Kalyuzhnaya MG, Yang S, Rozova ON, Smalley NE, Clubb J, Lamb A et al (2013) Highly efficient methane biocatalysis revealed in a methanotrophic bacterium. Nat Commun 4:2785
Kalyuzhnaya MG, Puri AW, Lidstrom ME (2015) Metabolic engineering in methanotrophic bacteria. Metab Eng 29:142–152
Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28(1):27–30
Kao WC, Chen YR, Eugene CY, Lee H, Tian Q, Wu KM, Tsai SF, Yu SS, Chen YJ, Aebersold R, Chan SI (2004) Quantitative proteomic analysis of metabolic regulation by copper ions in Methylococcus capsulatus (Bath). J Biol Chem 279(49):51554–51560
Karp PD, Latendresse M, Paley SM, Krummenacker M, Ong QD, Billington R et al (2015) Pathway tools version 19.0 update: software for pathway/genome informatics and systems biology. Brief Bioinform 17:bbv079
Karr JR, Sanghvi JC, Macklin DN, Gutschow MV, Jacobs JM, Bolival B, Assad-Garcia N, Glass JI, Covert MW (2012) A whole-cell computational model predicts phenotype from genotype. Cell 150(2):389–401
Khadem AF, Pol A, Wieczorek A, Mohammadi SS, Francoijs KJ, Stunnenberg HG et al (2011) Autotrophic methanotrophy in Verrucomicrobia: Methylacidiphilum fumariolicum SolV uses the Calvin-Benson-Bassham cycle for carbon dioxide fixation. J Bacteriol 193(17):4438–4446
Khadem AF, Wieczorek AS, Pol A, Vuilleumier S, Harhangi HR, Dunfield PF et al (2012) Draft genome sequence of the volcano-inhabiting thermoacidophilic methanotroph Methylacidiphilum fumariolicum strain SolV. J Bacteriol 194(14):3729–3730
Kitano H (ed) (2001) Foundations of systems biology. MIT Press, Cambridge, pp 1–36
Kits KD, Campbell DJ, Rosana AR, Stein LY (2015) Diverse electron sources support denitrification under hypoxia in the obligate methanotroph Methylomicrobium album strain BG8. Front Microbiol 6:1072
Klipp E, Herwig R, Kowald A, Wierling C, Lehrach H (2008) Systems biology in practice: concepts, implementation and application. Wiley, Weinheim
Larsen Ø, Karlsen OA (2016) Transcriptomic profiling of Methylococcus capsulatus (Bath) during growth with two different methane monooxygenases. Microbiologyopen 5(2):254–267
Laukel M, Rossignol M, Borderies G, Völker U, Vorholt JA (2004) Comparison of the proteome of Methylobacterium extorquens AM1 grown under methylotrophic and nonmethylotrophic conditions. Proteomics 4(5):1247–1264
Leak DJ, Dalton H (1983) In vivo studies of primary alcohols, aldehydes and carboxylic acids as electron donors for the methane mono-oxygenase in a variety of methanotrophs. Microbiology 129(11):3487–3497
Leak DJ, Dalton H (1986a) Growth yields of methanotrophs. Appl Microbiol Biotechnol 23(6):470–476
Leak DJ, Dalton H (1986b) Growth yields of methanotrophs 2. A theoretical analysis. Appl Microbiol Biotechnol 23(6):477–481
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(12):7503–7509
Lee SY, Kim HU (2015) Systems strategies for developing industrial microbial strains. Nat Biotechnol 33(10):1061–1072
Luesken FA, Wu ML, Op den Camp HJ, Keltjens JT, Stunnenberg H, Francoijs KJ, Strous M, Jetten MS (2012) Effect of oxygen on the anaerobic methanotroph ‘Candidatus Methylomirabilis oxyfera’: kinetic and transcriptional analysis. Environ Microbiol 14(4):1024–1034
Machado D, Herrgård M (2014) Systematic evaluation of methods for integration of transcriptomic data into constraint-based models of metabolism. PLoS Comput Biol 10(4):e1003580
Mast FD, Ratushny AV, Aitchison JD (2014) Systems cell biology. J Cell Biol 206(6):695–706
Matsen JB, Yang S, Stein LY, Beck DA, Kalyuzhanaya MG (2013) Global molecular analyses of methane metabolism in methanotrophic alphaproteobacterium, Methylosinus trichosporium OB3b. Part I: transcriptomic study. Front Microbiol 4:40
Op den Camp HJ, Islam T, Stott MB, Harhangi HR, Hynes A, Schouten S et al (2009) Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia. Environ Microbiol Rep 1(5):293–306
Orita I, Yurimoto H, Hirai R, Kawarabayasi Y, Sakai Y, Kato N (2005) The archaeon Pyrococcus horikoshii possesses a bifunctional enzyme for formaldehyde fixation via the ribulose monophosphate pathway. J Bacteriol 187(11):3636–3642
Orita I, Sato T, Yurimoto H, Kato N, Atomi H, Imanaka T, Sakai Y (2006) The ribulose monophosphate pathway substitutes for the missing pentose phosphate pathway in the archaeon Thermococcus kodakaraensis. J Bacteriol 188(13):4698–4704
Otto A, Becher D, Schmidt F (2014) Quantitative proteomics in the field of microbiology. Proteomics 14(4-5):547–565
Peyraud R, Kiefer P, Christen P, Massou S, Portais JC, Vorholt JA (2009) Demonstration of the ethylmalonyl-CoA pathway by using 13C metabolomics. Proc Natl Acad Sci 106(12):4846–4851
Peyraud R, Schneider K, Kiefer P, Massou S, Vorholt JA, Portais JC (2011) Genome-scale reconstruction and system level investigation of the metabolic network of Methylobacterium extorquens AM1. BMC Syst Biol 5(1):189
Rozova ON, But SY, Khmelenina VN, Reshetnikov AS, Mustakhimov II, Trotsenko YA (2017) Characterization of two recombinant 3-hexulose-6-phosphate synthases from the halotolerant obligate methanotroph Methylomicrobium alcaliphilum 20Z. Biochemistry (Mosc) 82(2):176–185
Sanchez-Osorio I, Ramos F, Mayorga P, Dantan E (2014) Foundations for modeling the dynamics of gene regulatory networks: a multilevel-perspective review. J Bioinform Comput Biol 12(01):1330003
Schellenberger J, Que R, Fleming RM, Thiele I, Orth JD, Feist AM et al (2011) Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox v2. 0. Nat Protoc 6(9):1290–1307
Semrau JD, DiSpirito AA, Yoon S (2010) Methanotrophs and copper. FEMS Microbiol Rev 34(4):496–531
Semrau JD, Jagadevan S, DiSpirito AA, Khalifa A, Scanlan J, Bergman BH et al (2013) Methanobactin and MmoD work in concert to act as the ‘copper-switch’ in methanotrophs. Environ Microbiol 15(11):3077–3086
Semrau JD, DiSpirito AA, Wenyu G, Yoon S, Cann I (2018) Metals and Methanotrophy. Appl Environ Microbiol 84(6):e02289-17
Sipkema EM, de Koning W, Ganzeveld KJ, Janssen DB, Beenackers AA (2000) NADH-regulated metabolic model for growth of Methylosinus trichosporium OB3b. Model presentation, parameter estimation, and model validation. Biotechnol Prog 16(2):176–188
Sirajuddin S, Rosenzweig AC (2015) Enzymatic oxidation of methane. Biochemistry 54(14):2283–2294
Tamas I, Smirnova AV, He Z, Dunfield PF (2014) The (d) evolution of methanotrophy in the Beijerinckiaceae—a comparative genomics analysis. ISME J 8(2):369
Tavormina PL, Kellermann MY, Antony CP, Tocheva EI, Dalleska NF, Jensen AJ, Dubilier N, Orphan VJ (2017) Starvation and recovery in the deep-sea methanotroph Methyloprofundus sedimenti. Mol Microbiol 103(2):242–252
Taylor SC, Dalton H, Dow CS (1981) Ribulose-1, 5-bisphosphate carboxylase/oxygenase and carbon assimilation in Methylococcus capsulatus (Bath). Microbiology 122(1):89–94
Torre A, Metivier A, Chu F, Laurens LM, Beck DA, Pienkos PT et al (2015) Genome-scale metabolic reconstructions and theoretical investigation of methane conversion in Methylomicrobium buryatense strain 5G (B1). Microb Cell Fact 14(1):1
Trotsenko YA, Murrell JC (2008) Metabolic aspects of aerobic obligate methanotrophy. Adv Appl Microbiol 63:183–229
Van Dien SJ, Lidstrom ME (2002) Stoichiometric model for evaluating the metabolic capabilities of the facultative methylotroph Methylobacterium extorquens AM1, with application to reconstruction of C3 and C4 metabolism. Biotechnol Bioeng 78(3):296–312
Van Oudenhove L, Devreese B (2013) A review on recent developments in mass spectrometry instrumentation and quantitative tools advancing bacterial proteomics. Appl Microbiol Biotechnol 97(11):4749–4762
Vorobev A, Jagadevan S, Jain S, Anantharaman K, Dick GJ, Vuilleumier S, Semrau JD (2014) Genomic and transcriptomic analyses of the facultative methanotroph Methylocystis sp. strain SB2 grown on methane or ethanol. Appl Environ Microbiol 80(10):3044–3052
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(10):2456–2463
Vuilleumier S, Chistoserdova L, Lee MC, Bringel F, Lajus A, Zhou Y et al (2009) Methylobacterium genome sequences: a reference blueprint to investigate microbial metabolism of C1 compounds from natural and industrial sources. PLoS One 4(5):e5584
Vuilleumier S, Khmelenina VN, Bringel F, Reshetnikov AS, Lajus A, Mangenot S et al (2012) Genome sequence of the haloalkaliphilic methanotrophic bacterium Methylomicrobium alcaliphilum 20Z. J Bacteriol 194(2):551–552
Ward N, Larsen Ø, Sakwa J, Bruseth L, Khouri H, Durkin AS et al (2004) Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2(10):e303
Wertz JT, Kim E, Breznak JA, Schmidt TM, Rodrigues JL (2012) Genomic and physiological characterization of the Verrucomicrobia isolate Diplosphaera colitermitum gen. nov., sp. nov., reveals microaerophily and nitrogen fixation genes. Appl Environ Microbiol 78(5):1544–1555
Yang S, Sadilek M, Lidstrom M (2012) Metabolite profiling and dynamic 13C metabolomics of one-carbon assimilation pathways in methylotrophic and methanotrophic bacteria. J Metabolomics Metab 1:2
Yang S, Matsen JB, Konopka M, Green-Saxena A, Clubb J et al (2013) Global molecular analyses of methane metabolism in methanotrophic Alphaproteobacterium, Methylosinus trichosporium OB3b. Part II. Metabolomics and 13C-labeling study. Front Microbiol 4:70
Yizhak K, Benyamini T, Liebermeister W, Ruppin E, Shlomi T (2010) Integrating quantitative proteomics and metabolomics with a genome-scale metabolic network model. Bioinformatics 26(12):i255–i260
Yoon S, Semrau JD (2008) Measurement and modeling of multiple substrate oxidation by methanotrophs at 20 C. FEMS Microbiol Lett 287(2):156–162
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Akberdin, I.R., Thompson, M., Kalyuzhnaya, M.G. (2018). Systems Biology and Metabolic Modeling of C1-Metabolism. In: Kalyuzhnaya, M., Xing, XH. (eds) Methane Biocatalysis: Paving the Way to Sustainability. Springer, Cham. https://doi.org/10.1007/978-3-319-74866-5_7
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