Priority pollutant degradation by the facultative methanotroph, Methylocystis strain SB2

Abstract

Methylocystis strain SB2, a facultative methanotroph capable of growth on multi-carbon compounds, was screened for its ability to degrade the priority pollutants 1,2-dichloroethane (1,2-DCA), 1,1,2-trichloroethane (1,1,2-TCA), and 1,1-dichloroethylene (1,1-DCE), as well as cis-dichloroethylene (cis-DCE) when grown on methane or ethanol. Methylocystis strain SB2 degraded 1,2-DCA and 1,1,2-TCA when grown on either substrate and cis-DCE when grown on methane. Growth of Methylocystis strain SB2 on methane was inhibited in the presence of all compounds, while only 1,1-DCE and cis-DCE inhibited growth on ethanol. No degradation of any chlorinated hydrocarbon was observed in ethanol-grown cultures when particulate methane monooxygenase (pMMO) activity was inhibited with the addition of acetylene, indicating that competition for binding to the pMMO between the chlorinated hydrocarbons and methane limited both methanotrophic growth and pollutant degradation when this strain was grown on methane. Characterization of Methylocystis strain SB2 found no evidence of a high-affinity form of pMMO for methane, nor could this strain utilize 1,2-DCA or its putative oxidative products 2-chloroethanol or chloroactetic acid as sole growth substrates, suggesting that this strain lacks appropriate dehydrogenases for the conversion of 1,2-DCA to glyoxylate. As ethanol: (1) can be used as an alternative growth substrate for promoting pollutant degradation by Methylocystis strain SB2 as the pMMO is not required for its growth on ethanol and (2) has been used to enhance the mobility of chlorinated hydrocarbons in situ, it is proposed that ethanol can be used to enhance both pollutant transport and biodegradation by Methylocystis strain SB2.

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References

  1. Baani M, Liesack W (2008) Two isozymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp strain SC2. Proceed Nat Acad Sciences 105:10203–10208

    Article  CAS  Google Scholar 

  2. Belova SE, Baani M, Suzina NE, Bodelier PLE, Liesack W, Dedysh SN (2011) Acetate utilization as a survival strategy of peat-inhabiting Methylocystis spp. Environ Microbiol Rep 3:36–46

    Article  CAS  Google Scholar 

  3. Blanksby SJ, Ellison GB (2003) Bond dissociation energies of organic molecules. Acc Chem Res 36:255–263

    Article  CAS  Google Scholar 

  4. Chang HL, Cohen LA (1996) Biodegradation of individual and multiple chlorinated aliphatic hydrocarbons by methane-oxidizing cultures. Appl Environ Microbiol 62:3371–3377

    CAS  Google Scholar 

  5. Dalton H, Stirling DI (1982) Co-metabolism. Phil Trans R Soc Lond 297:481–496

    Article  CAS  Google Scholar 

  6. Dedysh SN, Knief C, Dunfield PF (2005) Methylocella species are facultatively methanotrophic. J Bacteriol 187:4665–4670

    Article  CAS  Google Scholar 

  7. Dedysh SN, Panikov NS, Tiedje JM (1998) Acidophilic methanotrophic communities from sphagnum peat bogs. Appl Environ Microbiol 64:922–929

    CAS  Google Scholar 

  8. Dunfield PF, Belova SE, Vorob’ev AV, Cornish SL, Dedysh SN (2010) Methylocapsa aurea sp. nov., a facultative methanotroph possessing a particulate methane monooxygenase and emended description of the genus Methylocapsa. Intl J Syst Evol Microbiol 60:2659–2664

    Article  CAS  Google Scholar 

  9. Folkard GK (1986) The significance, occurrence and removal of volatile chlorinated hydrocarbon solvents in groundwaters. Wat Pollut Control 85:63–70

    CAS  Google Scholar 

  10. Hage JC, Hartmans S (1999) Monooxygenase-mediated 1,2-dichloroethane degradation by Pseudomonas sp. strain DCA1. Appl Environ Microbiol 65:2466–2470

    CAS  Google Scholar 

  11. Han JI, Semrau JD (2000) Chloromethane stimulates growth of Methylomicrobium album BG8 on methanol. FEMS Microbiol Lett 187:77–81

    Article  CAS  Google Scholar 

  12. Im J, Semrau JD (2011) Pollutant degradation by a Methylocystis strain SB2 grown on ethanol: bioremediation via facultative methanotrophy. FEMS Microbiol Lett 318:137–142

    Article  CAS  Google Scholar 

  13. Im J, Lee SW, Yoon S, DiSpirito AA, Semrau JD (2011) Characterization of a novel facultative Methylocystis species capable of growth on methane, acetate and ethanol. Environ Microbiol Rep 3:174–181

    Article  CAS  Google Scholar 

  14. Janssen DB, van der Ploeg JR, Pries F (1994) Genetics and biochemistry and 1,2-dichloroethane degradation. Biodegradation 5:249–257

    Article  CAS  Google Scholar 

  15. Janssen DB, Scheper A, Dijkhuizen D, Witholt B (1985) Degradation of halogenated aliphatic compounds by Xanthobacter autotrophicus GJ10. Appl Environ Microbiol 49:673–677

    CAS  Google Scholar 

  16. 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 72:7503–7509

    Article  CAS  Google Scholar 

  17. Murrell JC, McDonald IR, Gilbert B (2000) Regulation of expression of methane monooxygenases by copper ions. Trends Microbiol 8:221–225

    Article  CAS  Google Scholar 

  18. Paszczynski AJ, Paidisetti R, Johnson AK, Crawford RL, Colwell FS, Green T, Delwiche M, Lee H, Newby D, Brodie EL, Conrad M (2011) Proteomic and targeted qPCR analyses of subsurface microbial communities for presence of methane monooxygenase. Biodeg 22:1045–1059

    Article  CAS  Google Scholar 

  19. Rahman MT, Crombie A, Moussard H, Chen Y, Murrell JC (2011) Acetate repression of methane oxidation by supplemental Methylocella silvestris in a peat soil microcosm. Appl Environ Microbiol 77:4234–4236

    Article  CAS  Google Scholar 

  20. Ramakrishnan V, Ogram AV, Lindner A (2005) Impacts of co-solvent flushing on microbial populations capable of degrading trichloroethylene. Environ Health Persp 113:55–61

    Article  CAS  Google Scholar 

  21. Semrau JD, DiSpirito AA, Yoon S (2010) Methanotrophs and copper. FEMS Microbiol Rev 34:496–531

    CAS  Google Scholar 

  22. Semrau JD (2011) Bioremediation via methanotrophy: overview of recent findings and suggestions for future research. Front Microbiol 2:1–7

    Article  Google Scholar 

  23. Shukla AK, Vishwakarma P, Upadhyay SN, Tripathi AK, Prasana HC, Dubey SK (2009) Biodegradation of trichloroethylene (TCE) by methanotrophic community. Biores Technol 100:2469–2474

    Article  CAS  Google Scholar 

  24. Taylor TP, Rathfelder KM, Pennell KD, Abriola LM (2004) Effects of ethanol addition on micellar solubilization and plume migration during surfactant enhanced recovery of tetrachloroethene. J Contam Hydrology 69:73–99

    Article  CAS  Google Scholar 

  25. Theisen AR, Ali MH, Radajewski S, Dumont MG, Dunfield PF, McDonald IR, Dedysh SN, Miguez CB, Murrell JC (2005) Regulation of methane oxidation in the facultative methanotroph Methylocella silvestris BL2. Mol Microbiol 58:682–692

    Article  CAS  Google Scholar 

  26. Tse G, Orbey H, Sandler SI (1992) Infinite dilution activity coefficients and Henry’s law coefficients of some priority water pollutants determined by a relative gas chromatographic method. Environ Sci Technol 26:2017–2022

    Article  CAS  Google Scholar 

  27. van den Wijngaard AJ, Prins J, Smal AJAC, Janssen DB (1993) Degradation of 2-chloroethylvinylether by Ancylobacter aquaticus AD25 and AD27. Appl Environ Microbiol 59:2777–2783

    Google Scholar 

  28. van den Wijngaard AJ, van der Kamp WHJ, van der Ploeg J, Pries F, Kazemier B, Janssen DB (1992) Degradation of 1,2-dichloroethane by Ancylobacter aquaticus and other facultative methylotrophs. Appl Environ Microbiol 58:976–983

    Google Scholar 

  29. Van Hylckama Vlieg JET, Koning W, Janssen DB (1997) Effect of chlorinated ethene conversion on viability and activity of Methylosinus trichosporium OB3b. Appl Environ Microbiol 63:4961–4964

    Google Scholar 

  30. Whittenbury R, Phillips KC, Wilkinson JF (1970) Enrichment, isolation and some properties of methane-utilizing bacteria. J Gen Microbiol 61:205–218

    Article  CAS  Google Scholar 

  31. Yimga MT, Dunfield PF, Ricke P, Heyer J, Liesack W (2003) Wide distribution of a novel pmoA-like gene copy among type II methanotrophs, and its expression in Methylocystis strain SC2. Appl Environ Microbiol 69:5593–5602

    Article  CAS  Google Scholar 

  32. Yoon S, Im J, Bandow N, DiSpirito AA, Semrau JD (2011) Constitutive expression of pMMO by Methylocystis strain SB2 when grown on multi-carbon substrates: implications for biodegradation of chlorinated ethenes. Environ Microbiol Rep 3:182–188

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by the Office of Science (BER) US Department of Energy. We dedicate this manuscript to the memory of Professor Sir Howard Dalton, FRS (1944–2008) on the 30th anniversary of his construction of the definition of co-metabolism.

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Correspondence to Jeremy D. Semrau.

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Jagadevan, S., Semrau, J.D. Priority pollutant degradation by the facultative methanotroph, Methylocystis strain SB2. Appl Microbiol Biotechnol 97, 5089–5096 (2013). https://doi.org/10.1007/s00253-012-4310-y

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Keywords

  • Facultative methanotrophy
  • Methylocystis strain SB2
  • Chlorinated alkanes and alkenes
  • Biodegradation