Abstract
Despite the environmental relevance of CH4 and forthcoming stricter regulations, the development of cost-efficient and environmentally friendly technologies for CH4 abatement is still limited. To date, one of the most promising solutions for the mitigation of this important GHG consists of the bioconversion of CH4 into bioproducts with a high profit margin. In this context, methanotrophs have been already proven as cell-factories of some of the most expensive products synthesized by microorganisms. In the case of ectoine (1000 $ kg−1), already described methanotrophic genera such as Methylomicrobium can accumulate up to 20% (ectoine wt−1) using methane as the only carbon source. Moreover, α-methanotrophs, such as Methylosynus and Methylocystis, are able to store bioplastic concentrations up to 50–60% of their total cell content. More than that, methanotrophs are one of the greatest potential producers of methanol and exopolysaccharides. Although this methanotrophic factory could be enhanced throughout metabolic engineering, the valorization of CH4 into valuable metabolites has been already consistently demonstrated under continuous and discontinuous mode, producing more than one compound in the same bioprocess, and using both, single strains and specific consortia. This review states the state-of-the-art of this innovative biotechnological platform by assessing its potential and current limitations.
This is a preview of subscription content, log in via an institution to check access.
Reproduced with permission from Pastor et al. (2010). ectA encodes for the protein DABA acetyltransferase (EctA), ectB for diaminobutyric acid (DABA) aminotransferase (EctB), ectC for ectoine synthase (EctC) and ask for aspartokinase (Ask)
Similar content being viewed by others
References
Agren R, Liu L, Shoaie S et al (2013) The RAVEN toolbox and its use for generating a genome-scale metabolic model for Penicillium chrysogenum. PLoS Comput Biol 9(3):e1002980. https://doi.org/10.1371/journal.pcbi.1002980
Akberdin IR, Thompson M, Hamilton R et al (2018) Methane utilization in Methylomicrobium alcaliphilum 20ZR: a systems approach. Sci Rep 8:2512. https://doi.org/10.1038/s41598-018-20574-z
Anthony C (2011) How half a century of research was required to understand bacterial growth on C1 and C2 compounds; the story of the serine cycle and the ethylmalonyl-CoA pathway. Sci Prog 94:109–137
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(29):10203–10208
Bjorck CE, Dobson PD, Pandhal J (2018) Biotechnological conversion of methane to methanol: evaluation of progress and potential. AIMS Bioeng 5(1):1–38. https://doi.org/10.3934/bioeng.2018.1.1
Cal AJ, Sikkema WD, Ponce MI et al (2016) Methanotrophic production of polyhydroxybutyrate-co-hydroxyvalerate with high hydroxyvalerate content. Int J Biol Macromol 87:302–307. https://doi.org/10.1016/j.ijbiomac.2016.02.056
Campbell MA, Nyerges G, Kozlowski JA et al (2011) Model of the molecular basis for hydroxylamine oxidation and nitrous oxide production in methanotrophic bacteria. FEMS Microbiol Lett 322(1):82–89. https://doi.org/10.1111/j.1574-6968.2011.02340.x
Cantera S, Lebrero R, Rodríguez E et al (2017a) Continuous abatement of methane coupled with ectoine production by Methylomicrobium alcaliphilum 20Z in stirred tank reactors: a step further towards greenhouse gas biorefineries. J Clean Prod 152:134–141. https://doi.org/10.1016/j.jclepro.2017.03.123
Cantera S, Lebrero R, Rodríguez S et al (2017b) Ectoine bio-milking in methanotrophs: a step further towards methane-based bio-refineries into high added-value products. Chem Eng J 328:44–48. https://doi.org/10.1016/j.cej.2017.07.027
Cantera S, Muñoz R, Lebrero R et al (2018a) Technologies for the bioconversion of methane into more valuable products. Curr Opin Biotechnol 50:128–135
Cantera S, Sánchez-Andrea I, Lebrero R et al (2018b) Multi-production of high added market value metabolites from diluted methane emissions via methanotrophic extremophiles. Bioresour Technol 267:401–407. https://doi.org/10.1016/j.biortech.2018.07.057
Chistoserdova L, Kalyuzhnaya MG (2018) Current trends in methylotrophy. Trends Microbiol 26:703–714
Crombie A, Murrell C (2011) Chapter eight—development of a system for genetic manipulation of the facultative methanotroph Methylocella silvestris BL2. Methods Enzymol 495:119–133. https://doi.org/10.1016/B978-0-12-386905-0.00008-5
DiSpirito AA, Semrau JD, Murrell JC et al (2016) Methanobactin and the link between copper and bacterial methane oxidation. Microbiol Mol Biol Rev 80:387–409. https://doi.org/10.1128/MMBR.00058-15
Duan C, Luo M, Xing X (2011) High-rate conversion of methane to methanol by Methylosinus trichosporium OB3b. Bioresour Technol 102(15):7349–7353. https://doi.org/10.1016/j.biortech.2011.04.096
Freitas F, Alves VD, Reis MAM (2011) Advances in bacterial exopolysaccharides: from production to biotechnological applications. Trends Biotechnol 29(8):388–398
García-Pérez T, López JC, Passos F et al (2018) Simultaneous methane abatement and PHB production by Methylocystis hirsuta in a novel gas-recycling bubble column bioreactor. Chem Eng J 334:691–697. https://doi.org/10.1016/j.cej.2017.10.106
Ge X, Yang l, Sheets JP et al (2016) Biological conversion of methane to liquid fuels: status and opportunities. Biotechnol Adv 32:1460–1475
Han JS, Ahn CM, Mahanty B et al (2013) Partial oxidative conversion of methane to methanol through selective inhibition of methanol dehydrogenase in methanotrophic consortium from landfill cover soil. Appl Biochem Biotechnol 171(6):1487–1499. https://doi.org/10.1007/s12010-013-0410-0
Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60(2):439–471
Helm J, Wendlandt KD, Jechorek M et al (2008) Potassium deficiency results in accumulation of ultra-high molecular weight poly-β-hydroxybutyrate in a methane-utilizing mixed culture. J Appl Microbiol 105:1054–1061. https://doi.org/10.1111/j.1365-2672.2008.03831.x
Henry CS, DeJongh M, Best AA et al (2010) High-throughput generation, optimization and analysis of genome-scale metabolic models. Nat Biotechnol 28:977–982. https://doi.org/10.1038/nbt.1672
Hernández J, Gómez-Cuervo S, Omil F (2015) EPS and SMP as stability indicators during the biofiltration of diffuse methane emissions. Water Air Soil Pollut 226(10):1–12. https://doi.org/10.1007/s11270-015-2576-2
Hwang IY, Hur DH, Lee JH et al (2015) Batch conversion of methane to methanol using Methylosinus trichosporium OB3b as biocatalyst. J Microbiol Biotechnol 25(3):375–380. https://doi.org/10.4014/jmb.1412.12007
Kalyuzhnaya MG, Khmelenina V, Eshinimaev B et al (2008) Classification of halo (alkali) philic and halo (alkali) tolerant methanotrophs provisionally assigned to the genera Methylomicrobium and Methylobacter and emended description of the genus Methylomicrobium. Int J Syst Evol Microbiol 58:591–596
Karthikeyan OP, Chidambarampadmavathy K, Nadarajan S et al (2015) Effect of CH4/O2 ratio on fatty acid profile and polyhydroxybutyrate content in a heterotrophic-methanotrophic consortium. Chemosphere 141:235–242
Khmelenina VN, Kalyuzhnaya MG, Starostina NG et al (1997) Isolation and characterization of halotolerant alkaliphilic methanotrophic bacteria from Tuva Soda lakes. Curr Microbiol 35:257–261. https://doi.org/10.1007/s002849900249
Khmelenina VN, Sakharovskii VG, Reshetnikov AS et al (2000) Synthesis of osmoprotectants by halophilic and alkaliphilic methanotrophs. Microbiology 69:381
Khmelenina VN, Rozova ON, But SY et al (2015) Biosynthesis of secondary metabolites in methanotrophs: biochemical and genetic aspects (review). Appl Biochem Microbiol 51:150. https://doi.org/10.1134/S0003683815020088
Koller M, Maršálek L, de Sousa Dias MM et al (2017) Producing microbial polyhydroxyalkanoate (PHA) biopolyesters in a sustainable manner. New Biotechnol 37:24–38
Kunte HJ, Lentzen G, Galinski EA (2014) Industrial production of the cell protectant ectoine: protection mechanisms, processes, and products. Curr Biotechnol 3:10–25. https://doi.org/10.2174/22115501113026660037
Liu L, Agren R, Bordel S, Nielsen J (2010) Use of genome-scale metabolic models for understanding microbial physiology. FEBS Lett 584(12):2556–2564. https://doi.org/10.1016/j.febslet.2010.04.052
López JC, Arnáiz E, Merchán L et al (2018) Biogas-based polyhydroxyalkanoates production by Methylocystis hirsuta: a step further in anaerobic digestion biorefineries. Chem Eng J 333:529–536. https://doi.org/10.1016/j.cej.2017.09.185
Mahmoud AMA (2017) Biological conversion process of methane into methanol using mixed culture methanotrophic bacteria enriched from activated sludge system. Dissertation. University of York, Canada
Malashenko IP, Pirog TP, Romanovskaia V et al (2001) Search for methanotrophic producers of exopolysaccharides. Prikl Biokhim Mikrobiol 37:702–705. https://doi.org/10.1023/A:1012307202011
Methanol institute (2018a) The methanol industry. http://www.methanol.org/the-methanol-industry/. Accessed 27 Nov 2018
Methanol institute (2018b) Our members. https://www.methanol.org/our-members/. Accessed 27 Nov 2018
Mustakhimov II, Reshetnikov AS, Glukhov AS et al (2009) Identification and characterization of EctR1, a new transcriptional regulator of the ectoine biosynthesis genes in the halotolerant methanotroph Methylomicrobium alcaliphilum 20Z. J Bacteriol 192(2):410–417
Myung J, Flanagan JCA, Waymouth RM et al (2017) Expanding the range of polyhydroxyalkanoates synthesized by methanotrophic bacteria through the utilization of omega-hydroxyalkanoate co-substrates. AMB Express 7:118. https://doi.org/10.1186/s13568-017-0417-y
Nguyen AD, Hwang IY, Lee OK et al (2018) Systematic metabolic engineering of Methylomicrobium alcaliphilum 20Z for 2,3-butanediol production from methane. Metab Eng 47:323–333. https://doi.org/10.1016/j.ymben.2018.04.010
Nwodo UU, Green E, Okoh AI (2012) Bacterial exopolysaccharides: functionality and prospects. Int J Mol Sci 13:14002–14015
Pastor JM, Salvador M, Argandoña M et al (2010) Ectoines in cell stress protection: uses and biotechnological production. Biotechnol Adv 28:782–801. https://doi.org/10.1016/j.biotechadv.2010.06.005
Patil KR, Rocha I, Förster J, Nielsen J (2005) Evolutionary programming as a platform for in silico metabolic engineering. BMC Bioinform 6:308. https://doi.org/10.1186/1471-2105-6-308
Petersen LAH, Villadsen J, Jørgensen SB et al (2017) Mixing and mass transfer in a pilot scale U-loop bioreactor. Biotechnol Bioeng 114:344–354. https://doi.org/10.1002/bit.26084
Pieja AJ, Sundstrom ER, Criddle CS (2011) Poly-3-hydroxybutyrate metabolism in the type II methanotroph Methylocystis parvus OBBP. Appl Environ Microbiol 77(17):6012–6019. https://doi.org/10.1128/AEM.00509-11
Pieja AJ, Morse MC, Cal AJ (2017) Methane to bioproducts: the future of the bioeconomy? Curr Opin Chem Biol 41:123–131. https://doi.org/10.1016/j.cbpa.2017.10.024
Reshetnikov AS, Khmelenina VN, Trotsenko YA (2006) Characterization of the ectoine biosynthesis genes of haloalkalotolerant obligate methanotroph “Methylomicrobium alcaliphilum 20Z”. Arch Microbiol 184:286–297. https://doi.org/10.1007/s00203-005-0042-z
Reshetnikov AS, Khmelenina VN, Mustakhimov II et al (2011) Genes and enzymes of ectoine biosynthesis in halotolerant methanotrophs. Methods Enzymol 495:15–30. https://doi.org/10.1016/B978-0-12-386905-0.00002-4
Ritala A, Häkkinen ST, Toivari M et al (2017) Single cell protein—state-of-the-art, industrial landscape and patents 2001–2016. Front Microbiol 8:2009
Rostkowski KH, Pfluger AR, Criddle CS (2013) Stoichiometry and kinetics of the PHB-producing type II methanotrophs Methylosinus trichosporium OB3b and Methylocystis parvus OBBP. Bioresour Technol 132:71–77. https://doi.org/10.1016/j.biortech.2012.12.129
Sheets JP, Ge X, Li YF, Yu Z et al (2016) Biological conversion of biogas to methanol using methanotrophs isolated from solid-state anaerobic digestate. Bioresour Technol 201:50–57. https://doi.org/10.1016/j.biortech.2015.11.035
Simon R, Priefer U, Pühler A (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat Biotechnol 1:784–791. https://doi.org/10.1038/nbt1183-784
Stępniewska Z, Goraj W, Kuźniar A et al (2014) Biosynthesis of ectoine by the methanotrophic bacterial consortium isolated from Bogdanka coalmine (Poland). Appl Biochem Microbiol 50:594–600. https://doi.org/10.1134/S0003683814110039
Strong P, Laycock B, Mahamud S et al (2016a) The opportunity for high-performance biomaterials from methane. Microorganism 4:100–111. https://doi.org/10.3390/microorganisms4010011
Strong PJ, Kalyuzhnaya M, Silverman J et al (2016b) A methanotroph-based biorefinery: potential scenarios for generating multiple products from a single fermentation. Bioresour Technol 215:314–323. https://doi.org/10.1016/j.biortech.2016.04.099
Sugimori D, Takeguchi M, Okura I (1995) Biocatalytic methanol production from methane with Methylosinus trichosporium OB3b: an approach to improve methanol accumulation. Biotechnol Lett 17(8):783–784. https://doi.org/10.1007/BF00129004
Sundstrom ER, Criddle CS (2015) Optimization of methanotrophic growth and production of poly(3-hydroxybutyrate) in a high-throughput microbioreactor system. Appl Environ Microbiol 81(14):4767–4773
Torre 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/s12934-015-0377-3
Wendlandt KD, Jechorek M, Helm J et al (2001) Producing poly-3-hydroxybutyrate with a high molecular mass from methane. J Biotechnol 86:127–133. https://doi.org/10.1016/S0168-1656(00)00408-9
Wilshusen JH, Hettiaratchi JP, De Visscher A et al (2004) Methane oxidation and formation of EPS in compost: effect of oxygen concentration. Environ Pollut 129:305–314. https://doi.org/10.1016/j.envpol.2003.10.015
Xin JY, Zhang YX, Zhang S et al (2007) Methanol production from CO2 by resting cells of the methanotrophic bacterium Methylosinus trichosporium IMV 3011. J Basic Microbiol 47(5):426–435. https://doi.org/10.1002/jobm.200710313
Zhang T, Zhou J, Wang X et al (2016) Coupled effects of methane monooxygenase and nitrogen source on growth and poly-β-hydroxybutyrate (PHB) production of Methylosinus trichosporium OB3b. J Environ Sci 52:49–57. https://doi.org/10.1016/j.jes.2016.03.001
Zhen X, Wang Y (2015) An overview of methanol as an internal combustion engine fuel. Renew Sustain Energy Rev 52:477–493. https://doi.org/10.1016/j.rser.2015.07.083
Acknowledgements
This research was funded by the Spanish Ministry of Economy and Competitiveness, the European FEDER program and the European Commission (CTM2015-73228-JIN, H2020- MSCA-IF-2016: CH4BioVal-GA:750126 and Red NOVEDAR). The financial support from the regional government of Castilla y León and the Sustainable Processes Institute are also gratefully acknowledged (UIC71).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Cantera, S., Bordel, S., Lebrero, R. et al. Bio-conversion of methane into high profit margin compounds: an innovative, environmentally friendly and cost-effective platform for methane abatement. World J Microbiol Biotechnol 35, 16 (2019). https://doi.org/10.1007/s11274-018-2587-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-018-2587-4