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Environmental Science and Pollution Research

, Volume 25, Issue 17, pp 16816–16824 | Cite as

Characterization of toluene metabolism by methanotroph and its effect on methane oxidation

  • Ruo He
  • Yao Su
  • Ruo-Chan Ma
  • Shulin Zhuang
Research Article
  • 140 Downloads

Abstract

Methanotrophs not only oxidize CH4, but also can oxidize a relatively broad range of other substrates, including trichloroethylene, alkanes, alkenes, and aromatic compounds. In this study, Methylosinus sporium was used as a model organism to characterize toluene metabolism by methanotrophs. Reverse transcription quantitative PCR analysis showed that toluene enhanced the mmoX expression of M. sporium. When the toluene concentration was below 2000 mg m−3, the kinetics of toluene metabolism by M. sporium conformed to the Michaelis-Menten equation (Vmax = 0.238 g gdry weight−1 h−1, K m  = 545.2 mg m−3). The use of a solid-phase extraction technique followed by a gas chromatography-mass spectrometry analysis and molecular docking calculation showed that toluene was likely to primarily bind the di-iron center structural region of soluble methane monooxygenase (sMMO) hydroxylase and then be oxidized to o-cresol. Although M. sporium oxidized toluene, it did not incorporate toluene into its biomass. The coexistence of toluene and CH4 could influence CH4 oxidation, the growth of methanotrophs, and the distribution of CH4-derived carbon, which were related to the ratio of the toluene concentration to biomass. These results would be helpful to understand the metabolism of CH4 and non-methane volatile organic compounds in the environment.

Keywords

Methanotroph Methane monooxygenase Toluene Kinetics Methane-derived carbon 

Notes

Funding information

This work was financially supported by National Natural Science Foundation of China with Grant Nos. 41671245 and 41371012, Zhejiang Province Natural Science Foundation for Distinguished Young Scholars (LR13E080002).

References

  1. Allen MR, Braithwaite A, Hills CC (1997) Trace organic compounds in landfill gas at seven U.K. waste disposal sites. Environ Sci Technol 31:1054–1061CrossRefGoogle Scholar
  2. Alvarez-Cohen L, McCarty PL (1991) Product toxicity and cometabolic competitive inhibition modeling of chloroform and trichloroethylene transformation by resting methanotrophic resting cells. Appl Environ Microbiol 57:1031–1037Google Scholar
  3. Alvarez-Cohen L, Speitel GE (2001) Kinetics of aerobic cometabolism of chlorinated solvents. Biodegradation 12:105–126CrossRefGoogle Scholar
  4. Baik MH, Newcomb M, Friesner RA, Lippard SJ (2003) Mechanistic studies on the hydroxylation of methane by methane monooxygenase. Chem Rev 103:2385–2420CrossRefGoogle Scholar
  5. Bochevarov AD, Li JN, Song WJ, Friesener RA, Lippard SJ (2011) Insights into the different dioxygen activation pathways of methane and toluene monooxygenase hydroxylases. J Am Chem Soc 133:7384–7397CrossRefGoogle Scholar
  6. Bodelier PLE, Meima-Franke M, Hordijk CA, Steenbergh AK, Hefting MM, Bodrossy L, von Bergen M, Seifert J (2013) Microbial minorities modulate methane consumption through niche partitioning. ISME J 7:2214–2228CrossRefGoogle Scholar
  7. Bratbak G, Dundas I (1984) Bacteria dry matter content and biomass estimations. Appl Environ Microbiol 48:755–757Google Scholar
  8. Choi EJ, Jin HM, Lee SH, Math RK, Madsen EL, Jeon CO (2013) Comparative genomic analysis and benzene, toluene, ethylbenzene, and o-, m-, and p-xylene (BTEX) degradation pathways of Pseudoxanthomonas spadix BD-a59. Appl Environ Microbiol 79:663–671CrossRefGoogle Scholar
  9. Colby J, Stirling DI, Dalton H (1977) The soluble methane mono-oxygenase of Methylococcus capsulatus (Bath). Its ability to oxygenate n-alkanes, n-alkenes, ethers, and alicyclic, aromatic and heterocyclic compounds. Biochem J 165:395–402CrossRefGoogle Scholar
  10. Costello AM, Lidstrom ME (1999) Molecular characterization of functional and phylogenetic genes from natural populations of methanotrophs in lake sediments. Appl Environ Microbiol 65:5066–5074Google Scholar
  11. Coufal DE, Blazyk JL, Whittington DA, Wu WW, Rosenzweig AC, Lippard SJ (2000) Sequencing and analysis of the Methylococcus capsulatus (Bath) soluble methane monooxygenase genes. Eur J Biochem 267:2174–2185CrossRefGoogle Scholar
  12. Deutzmann JS, Hoppert M, Schink B (2014) Characterization and phylogeny of a novel methanotroph, Methyloglobulus morosus gen. Nov., spec. Nov. Syst Appl Microbiol 37:165–169CrossRefGoogle Scholar
  13. Dedysh SN, Dunfield PF (2011) Facultative and obligate methanotrophs: how to identify and differentiate them. Methods Enzymol 495:31–44CrossRefGoogle Scholar
  14. Ding K, Zhang H, Wang H, Lv X, Pan L, Zhang W, Zhuang S (2015) Atomic-scale investigation of the interactions between tetrabromobisphenol A, tetrabromobisphenol S and bovine trypsin by spectroscopies and molecular dynamics simulations. J Hazard Mater 299:486–494CrossRefGoogle Scholar
  15. Durmusoglu E, Taspinar F, Karademir A (2010) Health risk assessment of BTEX emissions in the landfill environment. J Hazard Mater 176:870–877CrossRefGoogle Scholar
  16. Fox BG, Borneman JG, Wackett LP, Lipscomb JD (1990) Haloalkene oxidation by the soluble methane monooxygenase from Methylosinus trichosporium OB3b: mechanistic and environmental implications. Biochemistry-US 29:6419–6427CrossRefGoogle Scholar
  17. Hanson RS, Hanson TE (1996) Methanotrophic bacteria. Microbiol Mol Biol Res 60:439–471Google Scholar
  18. He R, Ma RC, Yao XZ, Wei XM (2017) Response of methanotrophic activity to extracellular polymeric substance production and its influencing factors. Waste Manag 69:289–297.  https://doi.org/10.1016/j.wasman.2017.08.019 CrossRefGoogle Scholar
  19. Henry SM, Galic D (1991) Influence of endogenous and exogenous electron donors and trichloroethylene oxidation toxicity on trichloroethylene oxidation by methanotrophic cultures from a groundwater aquifer. Appl Environ Microbiol 57:236–244Google Scholar
  20. Jiang H, Chen Y, Jiang PX, Zhang C, Smith TJ, Murrell JC, Xing XH (2010) Methanotrophs: multifunctional bacteria with promising applications in environmental bioengineering. Biochem Eng J 49:277–288CrossRefGoogle Scholar
  21. Kong JY, Bai Y, Su Y, Yao YJ, He R (2014) Effects of trichloroethylene on community structure and activity of methanotrophs in landfill cover soils. Soil Biol Biochem 78:118–127CrossRefGoogle Scholar
  22. Lee EH, Park H, Cho KS (2010) Characterization of methane, benzene and toluene-oxidizing consortia enriched from landfill and riparian wetland soils. J Hazard Mater 184:313–320CrossRefGoogle Scholar
  23. Lee JY, Roh JR, Kim HS (1994) Metabolic engineering of Pseudomonas putida for the simultaneous biodegradation of benzene, toluene, and p-xylene mixture. Biotechnol Bioeng 43:1146–1152CrossRefGoogle Scholar
  24. Lieberman RL, Rosenzweig AC (2004) Biological methane oxidation: regulation, biochemistry, and active site structure of particulate methane monooxygenase. Crit Rev Biochem Mol 39:147–164CrossRefGoogle Scholar
  25. McDonald IR, Bodrossy L, Chen Y, Murrell JC (2008) Molecular ecology techniques for the study of aerobic methanotrophs. Appl Environ Microbiol 74:1305–1315CrossRefGoogle Scholar
  26. Mueller JG, Middaugh DP, Lantz SE, Chapman PJ (1991) Biodegradation of creosote and pentachlorphenol in contaminated groundwater: chemical and biological assessment. Appl Environ Microbiol 57:1277–1285Google Scholar
  27. Newman LM, Wackett LP (1995) Purification and characterization of toluene 2-monooxygenase from Burkholderia cepacia G4. Biochemistry 34:14066–14076CrossRefGoogle Scholar
  28. Nunes-Halldorson VDS, Steiner RL, Smith GB (2004) Residual toxicity after biodegradation: interactions among benzene, toluene, and chloroform. Ecotoxicol Environ Saf 57:162–167CrossRefGoogle Scholar
  29. Parales RE, Parales JV, Pelletier DA, Ditty JL (2008) Diversity of microbial toluene degradation pathways. Adv Appl Microbiol 64:1–73CrossRefGoogle Scholar
  30. Parker T, Dottridge J, Kelly S (2002) Investigation of the composition and emissions of trace components in landfill gas (P1–438/TR). Technical Report, Environment Agency, Bristol, UKGoogle Scholar
  31. Rataj MJ, Kauth JE, Donnelly MI (1991) Oxidation of deuterated compounds by high specific activity methane monooxygenase from Methylosinus trichosporium: mechanistic implications. J Biol Chem 266:18684–18690Google Scholar
  32. Saeki S, Mukaia S, Iwasaki K, Yagi O (1999) Production of trichloroacetic acid, trichloroethanol and dichloroacetic acid from trichloroethylene degradation by Methylocystis sp. strain M. Biocatal Biotransfor 17:347–357CrossRefGoogle Scholar
  33. Semrau JD, Dispirito AA, Yoon S (2010) Methanotrophs and copper. FEMS Microbiol Rev 34:496–531CrossRefGoogle Scholar
  34. Su Y, Xia FF, Tian BH, Li W, He R (2014a) Microbial community and function of enrichment cultures with methane and toluene. Appl Microbiol Biotechnol 98:3121–3131CrossRefGoogle Scholar
  35. Su Y, Zhang X, Wei XM, Kong JY, Xia FF, Li W, He R (2014b) Evaluation of simultaneous biodegradation of methane and toluene in landfill covers. J Hazard Mater 274:367–375CrossRefGoogle Scholar
  36. Su Y, Pei JS, Tian BH, Fan FX, Tang ML, Li W, He R (2015) Potential application of biocover soils to landfills for mitigating toluene emission. J Hazard Mater 229:18–26CrossRefGoogle Scholar
  37. Vorobev AV, Baani M, Doronina NV, Brady AL, Liesack W, Dunfield PF, Dedysh SN (2011) Methyloferula stellate gen. Nov., sp. nov., and acidophilic, obligately methanotrophic bacterium that possesses only a soluble methane monooxygenase. Int J Syst Evol Micr 61:2456–2463CrossRefGoogle Scholar
  38. Wang J, Xia FF, Bai Y, Fang CR, Shen DS, He R (2011) Methane oxidation in landfill waste biocover soil: kinetics and sensitivity to ambient conditions. Waste Manag 31:864–870CrossRefGoogle Scholar
  39. Wei XM, He R, Chen M, Su Y, Ma RC (2016) Conversion of methane-derived carbon and microbial community in enrichment cultures in response to O2 availability. Environ Sci Pollut R 23:7517–7528CrossRefGoogle Scholar
  40. Whittenbury R, Phillips KC, Wilkinson JF (1970) Enrichment, isolation and some properties of methane-utilising bacteria. J Gen Microbiol 61:205–218CrossRefGoogle Scholar
  41. Whittington DA, Sazinsky MH, Lippard SJ (2001) X-ray crystal structure of alcohol products bound at the active site of soluble monooxygenase hydroxylase. J Am Chem Soc 123:1794–1795CrossRefGoogle Scholar
  42. Wilkins PC, Dalton H, Samuel CJ, Green J (1994) Further evidence for multiple pathways in soluble methane-monooxygenase-catalysed oxidations from the measurement of deuterium kinetic isotope effects. Eur J Biochem 226:555–560CrossRefGoogle Scholar
  43. Yu H, Kim BJ, Rittmann BE (2001) The roles of intermediates in biodegradation of benzene, toluene and p-xylene by Pseudomonas putida F1. Biodegradation 12:455–463CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Environmental EngineeringZhejiang UniversityHangzhouChina
  2. 2.Institute of Environment, ResourceSoil and Fertilizer, Zhejiang Academy of Agricultural SciencesHangzhouChina
  3. 3.Institute of Environmental Science, College of Environmental and Resource SciencesZhejiang UniversityHangzhouChina

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