Kinetics and Stoichiometry of an Efficient Methanotroph Methylosarcina sp. LC-4 Isolated from a Municipal Solid Waste Dumpsite
Publication: Journal of Environmental Engineering
Volume 147, Issue 5
Abstract
In recent times methanotrophs have gained immense interest due to their ability to sequester and utilize methane, which is an inexpensive carbon source as well as a very potent greenhouse gas. Despite their vast potential for both industrial and environmental applications, only a few methanotrophs have been well studied to date. A novel and an efficient obligate methanotroph was isolated from a methanotrophic consortium originated from a municipal solid waste leachate. The isolate belonged to the genus Methylosarcina as confirmed by 16S ribosomal ribonucleic acid (rRNA) phylogenetic analysis and was further characterized by scanning electron microscopy, chemotaxonomic, and carbon, hydrogen, nitrogen, and sulphur (CHNS) elemental analysis. Methane oxidation by the isolate was studied in detail, including kinetics, specific oxygen requirement, and carbon capture efficiency. Further, the fate of oxidized methane was determined, unraveling its potential in the bioremediation of methane.
Get full access to this article
View all available purchase options and get full access to this article.
Data Availability Statement
All data generated or analyzed during the study are included in the published paper. There are no codes and models associated with this submission.
Acknowledgments
The authors acknowledge the Sophisticated Analytical Instrument facility (SAIF), IIT Madras for the SEM and CHNS analysis.
References
Albanna, M., and L. Fernandes. 2009. “Effects of temperature, moisture content, and fertilizer addition on biological methane oxidation in landfill cover soils.” J. Hazard. Toxic Radioact. Waste 13 (3): 187–195. https://doi.org/10.1061/(ASCE)1090-025X(2009)13:3(187.
AlSayed, A., A. Fergala, S. Khattab, and A. Eldyasti. 2018. “Kinetics of type I methanotrophs mixed culture enriched from waste activated sludge.” Biochem. Eng. J. 132 (Apr): 60–67. https://doi.org/10.1016/j.bej.2018.01.003.
Boiesen, A., E. Arvin, and K. Broholm. 1993. “Effect of mineral nutrients on the kinetics of methane utilization by methanotrophs.” Biodegradation 4 (3): 163–170. https://doi.org/10.1007/BF00695118.
Cabral, A. R., J. F. V. Moreira, and L.-B. Jugnia. 2010. “Biocover performance of landfill methane oxidation: Experimental results.” J. Environ. Eng. 136 (8): 785–793. https://doi.org/10.1061/(ASCE)EE.1943-7870.0000182.
Cáceres, M., A. D. Dorado, J. C. Gentina, and G. Aroca. 2017. “Oxidation of methane in biotrickling filters inoculated with methanotrophic bacteria.” Environ. Sci. Pollut. Res. Int. 24 (33): 25702–25712. https://doi.org/10.1007/s11356-016-7133-z.
Cai, Y., Y. Zheng, P. L. E. Bodelier, R. Conrad, and Z. Jia. 2016. “Conventional methanotrophs are responsible for atmospheric methane oxidation in paddy soils.” Nat. Commun. 7 (1): 1–10. https://doi.org/10.1038/ncomms11728.
Calhoun, A., and G. M. King. 1998. “Characterization of root-associated methanotrophs from three freshwater macrophytes: Pontederia cordata, Sparganium eurycarpum, and Sagittaria latifolia.” Appl. Environ. Microbiol. 64 (3): 1099–1105. https://doi.org/10.1128/AEM.64.3.1099-1105.1998.
Carlsen, H. N., L. Joergensen, and H. Degn. 1991. “Inhibition by ammonia of methane utilization in Methylococcus capsulatus (bath).” Appl. Environ. Microbiol. 35 (1): 124–127. https://doi.org/10.1007/BF00180649.
Dedysh, S. N., and P. F. Dunfield. 2014. “Hydrocarbon and lipid microbiology protocols cultivation of methanotrophs.” In Springer protocols handbooks, edited by T. J. McGenity, 231–247. Berlin: Springer.
Dunfield, P., and R. Conrad. 2000. “Starvation alters the apparent half-saturation constant for methane in the type II methanotroph Methylocystis strain LR1.” Appl. Environ. Microbiol. 66 (9): 4136–4138. https://doi.org/10.1128/AEM.66.9.4136-4138.2000.
Gilman, A., L. M. Laurens, A. W. Puri, F. Chu, P. T. Pienkos, and M. E. Lidstrom. 2015. “Bioreactor performance parameters for an industrially-promising methanotroph Methylomicrobium buryatense 5GB1.” Microb. Cell Fact. 14 (182): 1–8. https://doi.org/10.1186/s12934-015-0372-8.
Girard, M., A. A. Ramirez, G. Buelna, and M. Heitz. 2011. “Biofiltration of methane at low concentrations representative of the piggery industry—Influence of the methane and nitrogen concentrations.” Chem. Eng. J. 168 (1): 151–158. https://doi.org/10.1016/j.cej.2010.12.054.
Harwood, J. H., and S. J. Pirt. 1972. “Quantitative aspects of growth of the methane oxidizing bacterium Methylococcus capsulatus on methane in shake flask and continuous chemostat culture.” J. Appl. Bacteriol. 35 (4): 597–607. https://doi.org/10.1111/j.1365-2672.1972.tb03741.x.
Haubrichs, R., and R. Widmann. 2006. “Evaluation of aerated biofilter systems for microbial methane oxidation of poor landfill gas.” Waste Manage. 26 (4): 408–416. https://doi.org/10.1016/j.wasman.2005.11.008.
Hazeu, W., W. H. Batenburg-Van Der Vegte, and J. C. De Bruyn. 1980. “Some characteristics of Methylococcus mobilis sp. nov.” Arch. Microbiol. 124 (2–3): 211–220. https://doi.org/10.1007/BF00427729.
Huber-Humer, M., J. Gebert, and H. Hilger. 2008. “Biotic systems to mitigate landfill methane emissions.” Waste Manage. Res. 26 (1): 33–46. https://doi.org/10.1177/0734242X07087977.
Kalyuzhnaya, M. G. 2016a. Bergey’s manual of systematics of archaea and bacteria-methylosarcina. Edited by W. B. Whitman, F. Rainey, P. Kämpfer, M. Trujillo, J. Chun, P. DeVos, B. Hedlund, and S. Dedysh, 1–7. New York: Wiley.
Kalyuzhnaya, M. G. 2016b. Biotechnology for biofuel production and optimization—Methane biocatalysis: Selecting the right microbe. Edited by C. Eckert and C. T. Trinh, 353–383. Amsterdam, Netherlands: Elsevier.
Kalyuzhnaya, M. G., S. M. Stolyar, A. J. Auman, J. C. Lara, M. E. Lidstrom, and L. Chistoserdova. 2005. “Methylosarcina lacus sp. nov., a methanotroph from Lake Washington, Seattle, USA, and emended description of the genus Methylosarcina.” Int. J. Syst. Evol. Microbiol. 55 (6): 2345–2350. https://doi.org/10.1099/ijs.0.63405-0.
Kim, J., D. D. Kim, and S. Yoon. 2018. “Rapid isolation of fast-growing methanotrophs from environmental samples using continuous cultivation with gradually increased dilution rates.” Appl. Microbiol. Biotechnol. 102 (13): 5707–5715. https://doi.org/10.1007/s00253-018-8978-5.
Kirschke, S., et al. 2013. “Three decades of global methane sources and sinks.” Nat. Geosci. 6 (10): 813–823. https://doi.org/10.1038/ngeo1955.
Kwon, M., A. Ho, and S. Yoon. 2019. “Novel approaches and reasons to isolate methanotrophic bacteria with biotechnological potentials: Recent achievements and perspectives.” Appl. Microbiol. Biotechnol. 103 (1): 1–8. https://doi.org/10.1007/s00253-018-9435-1.
La, H., J. P. A. Hettiaratchi, G. Achari, and P. F. Dunfield. 2018. “Biofiltration of methane.” Bioresour. Technol. 268 (Nov): 759–772. https://doi.org/10.1016/j.biortech.2018.07.043.
Lamb, S. C., and J. C. Garver. 1980. “Batch- and continuous-culture studies of a methane-utilizing mixed culture.” Biotechnol. Bioeng. 22 (10): 2097–2118. https://doi.org/10.1002/bit.260221009.
Lawton, T. J., and A. C. Rosenzweig. 2016. “Methane-oxidizing enzymes: An upstream problem in biological gas-to-liquids conversion.” J. Am. Chem. Soc. 138 (30): 9327–9340. https://doi.org/10.1021/jacs.6b04568.
Leak, D. J., and H. Dalton. 1986. “Growth yields of methanotrophs. 1: Effect of copper on the energetics of methane oxidation.” Appl. Microbiol. Biotechnol. 23 (6): 470–476. https://doi.org/10.1007/BF02346062.
López, J. C., E. Porca, G. Collins, E. Clifford, G. Quijano, and R. Muñoz. 2019. “Ammonium influences kinetics and structure of methanotrophic consortia.” Waste Manage. 89 (Apr): 345–353. https://doi.org/10.1016/j.wasman.2019.04.028.
Mancebo, U., J. P. A. Hettiaratchi, and O. D. Hurtado. 2014. “Study on the correlation between dissolved organic carbon, specific oxygen uptake rate, and exchangeable nitrogen and the performance of granular materials as support media for methanotrophic biofiltration.” J. Hazard. Toxic Radioact. Waste 18 (1): 11–15. https://doi.org/10.1061/(ASCE)HZ.2153-5515.0000173.
Mao, T. T., R. Yin, and H. Deng. 2015. “Effects of copper on methane emission, methanogens and methanotrophs in the rhizosphere and bulk soil of rice paddy.” Catena 133 (Oct): 233–240. https://doi.org/10.1016/j.catena.2015.05.024.
Meraz, J. L., K. L. Dubrawski, S. H. El Abbadi, K.-H. Choo, and C. S. Criddle. 2020. “Membrane and fluid contactors for safe and efficient methane delivery in methanotrophic bioreactors.” J. Environ. Eng. 146 (6): 03120006. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001703.
Ordaz, A., J. C. López, I. Figueroa-González, R. Muñoz, and G. Quijano. 2014. “Assessment of methane biodegradation kinetics in two-phase partitioning bioreactors by pulse respirometry.” Water Res. 67 (Dec): 46–54. https://doi.org/10.1016/j.watres.2014.08.054.
Rodrigues, A., B. Valdman, and A. Salgado. 2009. “Analysis of methane biodegradation by Methylosinus trichosporium OB3b.” Braz. J. Microbiol. 40 (2): 301–307. https://doi.org/10.1590/S1517-838220090002000017.
Rostkowski, K. H., A. R. Pfluger, and C. S. Criddle. 2013. “Stoichiometry and kinetics of the PHB-producing type II methanotrophs Methylosinus trichosporium OB3b and Methylocystis parvus OBBP.” Bioresour. Technol. 132 (Mar): 71–77. https://doi.org/10.1016/j.biortech.2012.12.129.
Sadasivam, B. Y., and K. R. Reddy. 2014. “Landfill methane oxidation in soil and bio-based cover systems: A review.” Rev. Environ. Sci. Biotechnol. 13 (1): 79–107. https://doi.org/10.1007/s11157-013-9325-z.
Scheutz, C., P. Kjeldsen, J. E. Bogner, A. De Visscher, J. Gebert, H. A. Hilger, M. Huber-Humer, and K. Spokas. 2009. “Microbial methane oxidation processes and technologies for mitigation of landfill gas emissions.” Waste Manage. Res. 27 (5): 409. https://doi.org/10.1177%2F0734242X09339325.
Semrau, J. D. 2011. “Bioremediation via methanotrophy: Overview of recent findings and suggestions for future research.” Front. Microbiol. 2 (209): 1–7. https://doi.org/10.3389%2Ffmicb.2011.00209.
Shindell, D. T., G. Faluvegi, N. Bell, and G. A. Schmidt. 2005. “An emissions-based view of climate forcing by methane and tropospheric ozone.” Geophys. Res. Lett. 32 (4): L04803. https://doi.org/10.1029/2004GL021900.
Sipkema, E. M., W. De Koning, K. J. Ganzeveld, and D. B. Janssen. 1998. “Experimental pulse technique for the study of microbial kinetics in continuous culture.” J. Biotechnol. 64 (2–3): 159–176. https://doi.org/10.1016/S0168-1656(98)00076-5.
Sirajuddin, S., and A. C. Rosenzweig. 2015. “Enzymatic oxidation of methane.” Biochemistry 54 (14): 2283–2294. https://doi.org/10.1021/acs.biochem.5b00198.
Stein, V. B., J. P. A. Hettiaratchi, and G. Achari. 2001. “Numerical model for biological oxidation and migration of methane in soils.” J. Hazard. Toxic Radioact. Waste 5 (4): 225–234. https://doi.org/10.1061/(ASCE)1090-025X(2001)5:4(225).
Urmann, K., M. H. Schroth, M. Noll, G. Gonzalez-Gil, and J. Zeyer. 2008. “Assessment of microbial methane oxidation above a petroleum-contaminated aquifer using a combination of in situ techniques.” J. Geophys. Res. Biogeosci. 113 (2): G02006. https://doi.org/10.1029/2006JG000363.
Wise, M. G., J. V. Mcarthur, and L. J. Shimkets. 2001. “Methylosarcina fibrata gen. nov., sp. nov. and Methylosarcina quisquiliarum sp. nov., novel type I methanotrophs.” Int. J. Syst. Evol. Microbiol. 51 (2): 611–621. https://doi.org/10.1099/00207713-51-2-611.
Yang, T., W. Sun, and D. Yue. 2017. “Characterizing the effects of biologically active covers on landfill methane emission flux and bio-oxidation.” J. Environ. Eng. 143 (9): 04017059. https://doi.org/10.1061/(ASCE)EE.1943-7870.0001251.
Information & Authors
Information
Published In
Journal of Environmental Engineering
Volume 147 • Issue 5 • May 2021
Copyright
© 2021 American Society of Civil Engineers.
History
Received: Jul 30, 2020
Accepted: Dec 1, 2020
Published online: Feb 23, 2021
Published in print: May 1, 2021
Discussion open until: Jul 23, 2021
Authors
Metrics & Citations
Metrics
Citations
Download citation
If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.