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Applied Microbiology and Biotechnology

, Volume 85, Issue 2, pp 389–403 | Cite as

Effect of nutrient and selective inhibitor amendments on methane oxidation, nitrous oxide production, and key gene presence and expression in landfill cover soils: characterization of the role of methanotrophs, nitrifiers, and denitrifiers

  • Sung-Woo Lee
  • Jeongdae Im
  • Alan A. DiSpirito
  • Levente Bodrossy
  • Michael J. Barcelona
  • Jeremy D. SemrauEmail author
Environmental Biotechnology

Abstract

Methane and nitrous oxide are both potent greenhouse gasses, with global warming potentials approximately 25 and 298 times that of carbon dioxide. A matrix of soil microcosms was constructed with landfill cover soils collected from the King Highway Landfill in Kalamazoo, Michigan and exposed to geochemical parameters known to affect methane consumption by methanotrophs while also examining their impact on biogenic nitrous oxide production. It was found that relatively dry soils (5% moisture content) along with 15 mg NH 4 + (kg soil)−1 and 0.1 mg phenylacetylene∙(kg soil)−1 provided the greatest stimulation of methane oxidation while minimizing nitrous oxide production. Microarray analyses of pmoA showed that the methanotrophic community structure was dominated by Type II organisms, but Type I genera were more evident with the addition of ammonia. When phenylacetylene was added in conjunction with ammonia, the methanotrophic community structure was more similar to that observed in the presence of no amendments. PCR analyses showed the presence of amoA from both ammonia-oxidizing bacteria and archaea, and that the presence of key genes associated with these cells was reduced with the addition of phenylacetylene. Messenger RNA analyses found transcripts of pmoA, but not of mmoX, nirK, norB, or amoA from either ammonia-oxidizing bacteria or archaea. Pure culture analyses showed that methanotrophs could produce significant amounts of nitrous oxide, particularly when expressing the particulate methane monooxygenase (pMMO). Collectively, these data suggest that methanotrophs expressing pMMO played a role in nitrous oxide production in these microcosms.

Keywords

Methanotroph Landfill Nitrous oxide Methane Ammonia oxidizers 

Notes

Acknowledgements

We thank George Wells and Craig Criddle for providing an amoA amplicon from ammonia-oxidizing archaea. Support from the Department of Energy (DE-FC26-05NT42431) to JDS is also gratefully acknowledged.

References

  1. Amaral JA, Knowles R (1995) Growth of methanotrophs in methane and oxygen counter gradients. FEMS Microbiol Lett 126:215–220CrossRefGoogle Scholar
  2. Balasubramanian R, Rosenzweig AA (2008) Copper methanobactin: a molecule whose time has come. Curr Opin Chem Biol 12:1–5CrossRefGoogle Scholar
  3. Barlaz MA, Green RB, Chanton JP, Goldsmith CD, Hater GR (2004) Evaluation of a biologically active cover for mitigation of landfill gas emissions. Environ Sci Technol 38:4891–4899CrossRefGoogle Scholar
  4. Bender M, Conrad R (1995) Effect of CH4 concentrations and soil conditions on the induction of CH4 oxidation activity. Soil Biol Biochem 27:1517–1527CrossRefGoogle Scholar
  5. Bodelier PLE, Roslev P, Henckel T, Frenzel P (2000) Stimulation by ammonium-based fertilizers of methane oxidation in soil around rice plants. Nature 403:421–424CrossRefGoogle Scholar
  6. Bodrossy L, Stralis-Pavese N, Murrell JC, Radajewski S, Weilharter A, Sessitsch A (2003) Development and validation of a diagnostic microbial microarray for methanotrophs. Environ Microbiol 5:566–582CrossRefGoogle Scholar
  7. Boeckx P, Van Cleemput O (1996) Methane oxidation in a neutral cover soil: influence of moisture content, temperature, and nitrogen-turnover. J Environ Qual 25:178–183Google Scholar
  8. Boeckx P, Van Cleemput O, Villaralvo I (1996) Methane emission from a landfill and the methane oxidising capacity of its cover soil. Soil Biol Biochem 28:1397–1405CrossRefGoogle Scholar
  9. Bogner JE, Spokas KA, Burton EA (1997) Kinetics of methane oxidation in cover soil: temporal variations, a whole-landfill oxidation experiment, and modeling of net CH4 emissions. Environ Sci Technol 31:2504–2514CrossRefGoogle Scholar
  10. Braker G, Tiedje JM (2003) Nitric oxide reductases (norB) genes from pure cultures and environmental samples. Appl Environ Microbiol 69:3476–3483CrossRefGoogle Scholar
  11. Braker G, Fesefeldt A, Witzel K-P (1998) Development of PCR primer systems for amplification of nitrite reductases genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microbiol 64:3769–3775Google Scholar
  12. Brusseau GA, Tsien H-C, Hanson RS, Wackett LP (1990) Optimization of trichloroethylene oxidation by methanotrophs and the use of a colorimetric assay to detect soluble methane monooxygenase activity. Biodeg 1:19–29CrossRefGoogle Scholar
  13. Casciotti KL, Ward BB (2005) Phylogenetic analysis of nitric oxide reductases gene homologues from aerobic ammonia-oxidizing bacteria. FEMS Microb Ecol 52:197–205CrossRefGoogle Scholar
  14. Cebron A, Bodrossy L, Chen Y, Singer AC, Thompson IP, Prosser JI, Murrell JC (2007) Identity of active methanotrophs in landfill cover soil as revealed by DNA-stable isotope probing. FEMS Microbiol Ecol 62:12–23CrossRefGoogle Scholar
  15. Chan SI, Yu SSF (2008) Controlled oxidation of hydrocarbons by the membrane-bound methane monooxygenase: a case for a tricopper cluster. Acc Chem Res 41:969–979CrossRefGoogle Scholar
  16. Chen M, Ma LQ (2001) Comparison of three aqua regia digestion methods for twenty Florida soils. Soil Sci Soc Am J 65:491–499CrossRefGoogle Scholar
  17. Chen Y, Dumont MG, Cebron A, Murrell JC (2007) Identification of active methanotrophs in a landfill cover soil through detection of expression of 16S rRNA and functional genes. Environ Microbiol 9:2855–2869CrossRefGoogle Scholar
  18. Choi D-W, Kunz RC, Boyd ES, Semrau JD, Antholine WA, Han J-I et al (2003) The membrane-associated methane monooxygenase (pMMO) and pMMO-NADH:quinone oxidoreductase from Methylococcus capsulatus Bath. J Bacteriol 185:5755–5764CrossRefGoogle Scholar
  19. Choi D-W, Antholine WE, Do YS, Semrau JD, Kisting CJ, Kunz RC et al (2005) Effect of methanobactin on activity and electron paramagnetic resonance spectra of the methane oxidation by the membrane-associated methane monooxygenase in Methylococcus capsulatus Bath. Microbiology 151:3417–3426CrossRefGoogle Scholar
  20. Choi D-W, Zea CJ, Do YS, Semrau JD, Antholine WA, Hargrove MS et al (2006) Spectral, kinetic and thermodynamic properties of Cu(I)- and Cu(II)-binding by methanobactin from Methylosinus trichosporium OB3b. Biochemistry 45:1142–1153Google Scholar
  21. 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
  22. Coyne MS, Tiedje JM (1990) Induction of denitrifying enzymes in oxygen-limited Achromobacter cyclolastes continuous culture. FEMS Microbiol Ecol 73:263–270CrossRefGoogle Scholar
  23. Czepiel PM, Mosher B, Crill PM, Hariss RC (1996) Quantifying the effect of oxidation on landfill emissions. J Geophys Res 101:16721–16729CrossRefGoogle Scholar
  24. Dantata N, Touran A, Wang J (2005) An analysis of cost and duration for deconstruction and demolition of residential buildings in Massachusetts. Resour Conserv Recycl 44:1–15CrossRefGoogle Scholar
  25. De Visscher A, Van Cleemput O (2003) Induction of enhanced CH4 oxidation in soils: NH4+ inhibition patterns. Soil Biol Biochem 35:907–913CrossRefGoogle Scholar
  26. Dedysh SN, Liesack W, Khmelenina VN, Suzina NE, Trotsenko YA, Semrau JD, Bares AM, Panikov NS, Tiedje JM (2000) Methylocella palustris gen. nov., sp. nov., a new methane-oxidizing acidophilic bacterium from peat bogs, representing a novel subtype of serine-pathway methanotrophs. Intl J Syst Evol Microbiol 50:955–969Google Scholar
  27. DeVisscher A, Boeckx P, van Cleemput O (2007) Artificial methane sinks. In: Reay DS, Hewitt CN, Grace J (eds) Greenhouse gas sinks. Wallingford, Oxfordshire, pp 184–200Google Scholar
  28. El Masri AM, Smith JN, Williams RT (1958) Studies in detoxication, 73. The metabolism of alkylbenzenes: phenylacetylene and phenylethylene (styrene). Biochem J 68:199–204Google Scholar
  29. Energy Information Administration (2008) Emission of greenhouse gases in the United States 2007. Office of Integrated Analysis and Forecasting, US Department of Energy, Washington DC 20585. Available at http://www.eia.doe.gov/oiaf/1605/ggrpt/pdf/0573(2007).pdf
  30. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Nat Acad Sci 102:14683–14688CrossRefGoogle Scholar
  31. Hakemian AS, Kondapalli KC, Tesler J, Hoffman BM, Stemmler TL, Rosenzweig AC (2008) The metal centers of particulate methane monooxygenase from Methylosinus trichosporium OB3b. Biochemistry 47:6793–6801CrossRefGoogle Scholar
  32. Hallin S, Lindgren P-E (1999) PCR detection of genes encoding nitrite reductases in denitrifying bacteria. Appl Environ Microbiol 65:1652–1657Google Scholar
  33. Han JI, Semrau JD (2004) Quantification of gene expression in methanotrophs by competitive reverse transcription-polymerase chain reaction. Environ Microbiol 6:388–399CrossRefGoogle Scholar
  34. Hilger H, Barlaz M, Wollum A (2000) Landfill CH4 oxidation: response to vegetation, fertilization and liming. J Environ Qual 29:324–334Google Scholar
  35. Holmes AJ, Costello A, Lidstrom ME, Murrell JC (1995) Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionary related. FEMS Microbiol Lett 132:203–208CrossRefGoogle Scholar
  36. Hooper AB, Terry KR (1979) Hydroxylamine oxidoreductase of Nitrosomonas production of nitric oxide from hydroxylamine. Biochim Biophys Acta 571:12–20Google Scholar
  37. Hou AX, Chen GX, Wang ZP, Van Cleemput O, Patrick WH (2000) Methane and nitrous oxide emissions from a rice field in relation to soil redox and microbiological processes. Soil Sci Am J 64:2180–2186Google Scholar
  38. Hutchens E, Radajewski S, Dumont MG, McDonald IR, Murrell JC (2004) Analysis of methanotrophic bacteria in Movile Cave by stable isotope probing. Environ Microbiol 6:111–120CrossRefGoogle Scholar
  39. IPCC (2007) Climate change 2007: synthesis report. Cambridge University Press, CambridgeGoogle Scholar
  40. Jiang Q-Q, Bakken LR (1999) Nitrous oxide production and methane oxidation by different ammonia-oxidizing bacteria. Appl Environ Microbiol 65:2679–2684Google Scholar
  41. Jones HA, Nedwell DB (1993) Methane emission and methane oxidation in land-fill cover soil. FEMS Microbiol Ecol 102:185–195CrossRefGoogle Scholar
  42. Kightley D, Nedwell DB, Cooper M (1995) Capacity for methane oxidation in landfill cover soils measured in laboratory-scale soil microcosms. Appl Environ Microbiol 61:592–601Google Scholar
  43. Knapp WC, Fowle DA, Kulcycki E, Roberts JA, Graham DW (2007) Methane monooxygenase gene expression mediated by methanobactin in the presence of mineral copper sources. Proc Natl Acad Sci USA 104:12040–12045CrossRefGoogle Scholar
  44. Krämer M, Baumgartner M, Bender M, Conrad R (1990) Consumption of NO by methanotrophic bacteria in pure culture and in soil. FEMS Microbiol Ecol 73:345–350CrossRefGoogle Scholar
  45. Kreader CA (1996) Relief of amplification inhibition in PCR with bovine serum albumin or T4 gene 32 protein. Appl Environ Microbiol 62:1102–1106Google Scholar
  46. Kucera I (2006) Interference of chlorate and chlorite with nitrate reduction in resting cells of Paracoccus denitrificans. Microbiol-SGM 152:3529–3534CrossRefGoogle Scholar
  47. Kulczycki E, Fowle DA, Knapp C, Graham DW, Roberts JA (2007) Methanobactin-promoted dissolution of Cu-substituted borsilicate glass. Geobiology 5:251–263CrossRefGoogle Scholar
  48. Lee S-W, Keeney DR, Lim D-H, 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 72:7503–7509CrossRefGoogle Scholar
  49. Leiberman RL, Rosenzweig AC (2005) Crystal structure of a membrane-bound metalloenzyme that catalyzes the biological oxidation of methane. Nature 434:177–182CrossRefGoogle Scholar
  50. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW et al (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809CrossRefGoogle Scholar
  51. Lontoh S, Semrau JD (1998) Trichloroethylene and methane oxidation by the particulate methane monooxygenase of Methylosinus trichosporium OB3b. Appl Environ Microbiol 64:1106–1114Google Scholar
  52. Lontoh S, DiSpirito AA, Krema CL, Whittaker MR, Hooper AB, Semrau JD (2000) Differential inhibition in vivo of ammonia monooxygenase, soluble methane monooxygenase and membrane-associated methane monooxygenase by phenylacetylene. Environ Microbiol 2:485–494CrossRefGoogle Scholar
  53. Majumdar D (2003) Methane and nitrous oxide emission from irrigated rice fields: proposed mitigation strategies. Curr Sci 84:1317–1326Google Scholar
  54. Martinho M, Choi DW, DiSpirito AA, Antholine WE, Semrau JD, Münck (2007) Mössbauer studies of the membrane-associated methane monooxygenase from Methylococcus capsulatus Bath: evidence or a diiron center. J Am Chem Soc 129:15783–15785CrossRefGoogle Scholar
  55. McBride MB, Richards BK, Steenhuis T (2004) Bioavailability and crop uptake of trace elements in soil columns amended with sewage sludge products. Plant Soil 262:71–84CrossRefGoogle Scholar
  56. Nishimura S, Sawamoto T, Akiyama H, Sudo S, Yagi K (2004) Methane and nitrous oxide emissions from a paddy field with Japanese conventional water management and fertilizer application. Global Biogeochem Cycles 18:2207–2216CrossRefGoogle Scholar
  57. Poth M, Focht DD (1985) 15N kinetic analysis of N2O production by Nitrosomonas europaea: an examination of nitrifier denitrification. Appl Environ Microbiol 49:1134–1141Google Scholar
  58. Prior SD, Dalton H (1985) The effect of copper ions on the membrane content and methane monooxygenase activity in methanol grown cells of Methylococcus capsulatus (Bath). J Gen Microbiol 131:155–163Google Scholar
  59. Qian X, Koerner RM, Gray DH (2002) Geotechnical aspects of landfill design and construction. Prentice-Hall, Inc, Upper Saddle RiverGoogle Scholar
  60. Reay DS, Smith KA, Hewitt CN (2007) Methane: importance, source and sinks. In: Reay DS, Hewitt CN, Grace J (eds) Greenhouse gas sinks. Wallingford, Oxfordshire, pp 143–151Google Scholar
  61. Ren T, Roy R, Knowles R (2000) Production and consumption of nitric oxide by three methanotrophic bacteria. Appl Environ Microbiol 66:3891–3897CrossRefGoogle Scholar
  62. Rinne J, Pihlatie M, Lohila A, Thum T, Aurela M, Tuovinen J-P, Laurila T, Vesala T (2005) Nitrous oxide emissions from a municipal landfill. Env Sci Technol 39:7790–7793CrossRefGoogle Scholar
  63. Ritchie GA, Nicholas DJD (1972) Identification of the sources of nitrous oxide produced by oxidative and reductive processes in Nitrosomonas europaea. Biochem J 126:1181–1191Google Scholar
  64. Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker, molecular fine scale analysis of natural ammonia oxidizing populations. Appl Environ Microbiol 63:4704–4712Google Scholar
  65. Rusmana I, Nedwell DB (2004) Use of chlorate as a selective inhibitor to distinguish membrane-bound nitrate reductases (Nar) and periplasmic nitrate reductases (Nap of dissimilative nitrate reducing bacteria in sediment. FEMS Micobiol Ecol 48:379–386CrossRefGoogle Scholar
  66. Seghers D, Siciliano SD, Top EM, Verstraete W (2005) Combined effect of fertilizer and herbicide applications on the abundance, community structure and performance of the soil methanotrophic community. Soil Biol Biochem 37:187–193CrossRefGoogle Scholar
  67. Shaw LJ, Nicol GW, Smith Z, Fear J, Prosser JI, Baggs EM (2006) Nitrosospira spp. can produce nitrous oxide via a nitrifier denitrification pathway. Environ Microbiol 8:214–222CrossRefGoogle Scholar
  68. Soil Survey Division Staff (1993) Soil survey manual. U.S. Department of Agriculture Handbook 18. U.S. Government Printing Office, Washington DCGoogle Scholar
  69. Stanley SH, Dalton H (1983) Copper stress underlies the fundamental change in intracellular location of methane mono-oxygenase in methane utilizing organisms: studies in batch and continuous cultures. Biotechnol Lett 5:487–492CrossRefGoogle Scholar
  70. Stralis-Pavese N, Sessitsch S, Weilharter A, Reichenauer T, Riesing J, Csontos J et al (2004) Optimization of diagnostic microarray for application in analysing landfill methanotrophic communities under different plant covers. Environ Microbiol 6:347–363CrossRefGoogle Scholar
  71. Sutka RL, Ostrom NE, Ostrom PH, Gandhi H, Breznak JA (2003) Nitrogen isotopomer site preference of N2O produced by Nitrosomonas europaea and Methylococcus capsulatus Bath. Rapid Commun Mass Spectrom 17:738–745CrossRefGoogle Scholar
  72. Sutka RL, Ostrom NE, Ostrom PH, Breznak JA, Gandhi H, Pitt AJ, Li F (2006) Distinguishing nitrous oxide production from nitrification and denitrification on the basis of isotopomer abundances. Appl Environ Microbiol 72:638–644CrossRefGoogle Scholar
  73. US EPA (1996) Standards of performance for new stationary sources and guidelines for control of existing sources: municipal solid waste landfills. Code of Federal Regulations, Title 40, Sections 9, 51, 52, and 60; Fed Regist 61 (49)Google Scholar
  74. Whalen SC, Reeburgh WS (1990) Consumption of atmospheric methane by tundra soils. Nature 346:160–162CrossRefGoogle Scholar
  75. Whalen SC, Reeburgh WS, Sandbeck KA (1990) Rapid methane oxidation in a landfill cover soil. Appl Environ Microbiol 56:3405–3411Google Scholar
  76. Whittenbury RK, Philips KD, Wilkinson JF (1970) Enrichment, isolation, and characterization of methane-utilizing bacteria. J Gen Microbiol 61:205–218Google Scholar
  77. Yoshinari T (1985) Nitrite and nitrous oxide production by Methylosinus trichosporium. Can J Microbiol 31:139–144CrossRefGoogle Scholar
  78. Zahn JA, DiSpirito AA (1996) Membrane-associated methane monooxygenase from Methylococcus capsulatus Bath. J Bacteriol 178:1018–1029Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Sung-Woo Lee
    • 1
    • 5
  • Jeongdae Im
    • 1
  • Alan A. DiSpirito
    • 2
  • Levente Bodrossy
    • 3
  • Michael J. Barcelona
    • 4
  • Jeremy D. Semrau
    • 1
    Email author
  1. 1.Department of Civil and Environmental EngineeringThe University of MichiganAnn ArborUSA
  2. 2.Department of Biochemistry, Biophysics and Molecular BiologyIowa State UniversityAmesUSA
  3. 3.Department of BiotechnologyARC Seibersdorf Research GmbHSeibersdorfAustria
  4. 4.Department of ChemistryWestern Michigan UniversityKalamazooUSA
  5. 5.Oregon Graduate Institute, Department of Environmental and Biomolecular SystemsOregon Health and Sciences UniversityBeavertonUSA

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