Publikationsserver der Universitätsbibliothek Marburg

Titel:Methane oxidizing bacteria at the oxic-anoxic interface : taxon-specific activity and resilience
Autor:Reim, Andreas
Weitere Beteiligte: Frenzel, Peter (Prof. Dr.)
Veröffentlicht:2012
URI:https://archiv.ub.uni-marburg.de/diss/z2013/0124
DOI: https://doi.org/10.17192/z2013.0124
URN: urn:nbn:de:hebis:04-z2013-01243
DDC: Biowissenschaften, Biologie
Titel (trans.):Methan oxidierende Bakterien an der oxisch-anoxischen Grenzschicht
Publikationsdatum:2013-04-12
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
Methan, Methan, Paddy, pmoA, Methanstoffwechsel, pmoA

Summary:
The methanotrophic bacteria are the only known biological sink for the third most important greenhouse gas methane, performing an important ecosystem function influencing global climate change. In the soil surface layer of water logged soils aerobic methanotrophs thrive at the oxic-anoxic interface attenuating the amount of potentially emitted methane. The highly diverse methanotroph community is shaping the interface characterized by overlapping methane and oxygen gradients by their own activity. However, how the different methanotrophs physically share their microhabitat at the interface is unknown. Here we highly resolved the vertical distribution and activity of methanotrophs at the interface. To assess the structure of the present and active methanotroph community the particulate methane monooxygenase gene pmoA was used as a functional and phylogenetic marker. For quantification of pmoA genes and transcripts a new method, the competitive-(reverse transcriptase)-t-RFLP was established. Only a subset of the methanotroph community was shown to be active and the major activity was confined to a small zone around the interface. The predominantly active methanotrophs were affiliated to Methylobacter and no transcripts of type II methanotrophs (Methylosinus, Methylocystis) were found. Hence, different species within this guild exploited different niches in the same microenvironment. Furthermore, the methanotrophs resistance to desciccation (up to 18 years) was tested. Longer-lasting droughts reduced methanotrophic diversity, and adversely affected methane oxidation upon rewetting. Type I methanotrophs showed relatively higher pmoA gene expression, while type II were more resistant to desiccation. Finally, we showed that high methane source strength aids the ability of the methanotroph community to recover from the effect of a strong disturbance. However, recovery of the type II community was independent of pmoA gene expression and source strength indicating facultative growth. Overall, the methanotroph community in the soil surface layer is highly diverse. This work contributed to understand the high and apparently redundant diversity by unravelling niche differentiation at the fine spatial resolution and evaluating the effect of different source strength. Moreover, the range of alternative substrates used for growth seems to be another important factor in the environment.

Bibliographie / References

  1. Horz,H.P., Rich,V., Avrahami,S., and Bohannan,B.J.M. (2005) Methane-oxidizing bacteria in a California upland grassland soil: diversity and response to simulated global change. Appl. Environ. Microbiol. 71: 2642-2652.
  2. References Bodrossy, L., Stralis-Pavese, N., Konrad-Koszler, M., Weilharter, A., Reichenauer, T.G., Schofer, D., and Sessitsch, A. (2006) mRNA-based parallel detection of active methanotroph populations by use of a diagnostic microarray. Appl Environ Microbiol 72: 1672-1676.
  3. Lüke, C., and Frenzel, P. (2011) Potential of pmoA amplicon pyrosequencing for methanotroph diversity studies. Appl Environ Microbiol 77: 6305-6309.
  4. Trotsenko, Y.A., and Murrell, J.C. (2008) Metabolic aspects of aerobic obligate methanotrophy. Adv Appl Microbiol 63: 183-229.
  5. Steenbergh, A.K., Meima, M.M., Kamst, M., and Bodelier, P.L.E. (2010) Biphasic kinetics of a methanotrophic community is a combination of growth and increased activity per cell. FEMS Microbiol Ecol 71: 12-22.
  6. Semrau, J.D., DiSpirito, A. A., and Yoon, S. (2010) Methanotrophs and copper. FEMS Microbiol Rev 34: 496-531.
  7. Ho,A., Kerckhof,F.M., Lüke,C., Reim,A., Krause,S., Boon,N., and Bodelier,P.L.E. (2012) Conceptualizing functional traits and ecological characteristics of methane-oxidizing bacteria as life strategies. Environ. Microbiol. Rep. doi: 10.1111/j.1758-2229.2012.00370.x BEITRÄGE ZU WISSENSCHAFTLICHEN TAGUNGEN Andreas Reim; " pmoA copy quantification via competitive PCR " ; 1 st MECOMECON Project Meeting; May 2010; Nieuwersluis, the Netherlands (Oral presentation)
  8. Bodelier,P.L.E., Bär-Gillesen,M.J., Meima-Franke,M., and Hordijk,K. (2012) Structural and functional response of methane-consuming microbial communities to different flooding regimes in riparian soils. Ecology and Evolution 2: 106-127.
  9. Verstraete, W., Wittebolle, L., Heylen, K., Vanparys, B., de Vos, P., van de W iele, T., and Boon, N. (2007) Microbial resource management: the road to go for environmental biotechnology. Eng Life Sci 7: 117-126.
  10. Rothfuss,F., Bender,M., and Conrad,R. (1997) Survival and activity of bacteria in a deep, aged lake sediment (Lake Constance). Microb. Ecol. 33: 69-77.
  11. Paszczynski, A.J., Paidisetti, R., Johnson, A.K., Crawford, R.L, Colwell, F.S., Green, T., et al. (2011) Proteomic and targeted qPCR analyses of subsurface microbial communities for presence of methane monooxygenase. Biodegrad 23: 1045-1059.
  12. Singh,J.S., Raghubanshi,A.S., Reddy,V.S., Singh,S., and Kashyap,A.K. (1998) Methane flux from irrigated paddy and dryland rice fields, and from seasonally dry tropical forest and savanna soils of india. Soil Biol. Biochem. 30: 135-139.
  13. Singh,S., Singh,J.S., and Kashyap,A.K. (1999) Methane consumption by soils of dryland rice agriculture: influence of varieties and N-fertilization. Chemosphere 38: 175-189.
  14. Rigby, M., Prinn, R.G., Fraser, P.J., Simmonds, P.G., Langenfelds, R.L., Huang, J., et al. (2008) Renewed growth of atmospheric methane. Geophys Res Lett 35: 1-6.
  15. Rahman, T., Crombie, A., Chen, Y., Stralis-Pavese, N., Bodrossy, L., Meir, P., McNamara, N., and Murrell, C. (2011) Environmental distribution and abundance of the facultative methanotroph Methylocella. ISME J 5: 1061-1066.
  16. Shrestha, M., Shrestha, P.M., Frenzel, P., and Conrad, R. (2010) Effect of nitrogen fertilization on methane oxidation, abundance, community structure, and gene expression of methanotrophs in the rice rhizosphere. ISME J 4: 1545-1556.
  17. Singh, B.K., Bardgett, R.D., Smith, P., and Reay, D.S. (2010) Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nature Rev 8:779-790.
  18. References Henckel, T., Roslev, P., and Conrad, R. (2000) Effects of O 2 and CH 4 on presence and activity of the indigenous methanotrophic community in rice field soil. Environ Microbiol 2: 666-679.
  19. Knapp, C.W., Fowle, D.A., Kulczycki, E., Roberts, J.A., and Graham, D.W. (2007) Methane monooxygenase gene expression mediated by methanobactin in the presence of mineral copper sources. Proc Natl Acad Sci USA 104: 12040-12045.
  20. Orphan, V.J., House, C.H., Hinrichs, K.U., McKeegan, K.D., and DeLong, E.F. (2002) Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. Proc Natl Acad Sci USA 99: 7663-7668.
  21. Grime,J.P. (1977) Evidence for the Existence of Three Primary Strategies in Plants and Its Relevance to Ecological and Evolutionary Theory. The American Naturalist 111: 1169- 1194.
  22. Dedysh,S.N., Khmelenina,V.N., Suzina,N.E., Trotsenko,Y.A., Semrau,J.D., Liesack,W., and Tiedje,J.M. (2002) Methylocapsa acidiphila gen. nov., sp. nov., a novel methane- oxidizing and dinitrogen-fixing acidophilic bacterium from Sphagnum bog. Int. J. Syst. Evol. Microbiol. 52: 251-261.
  23. Knief, C., and Dunfield, P. (2005) Response and adaptation of different methanotrophic bacteria to low methane mixing ratios. Environ Microbiol 7: 1307-1317.
  24. Dumont, M.G., Pommerenke, B., Casper, P., and Conrad, R. (2011) DNA-, rRNA-and mRNA-based stable isotope probing of aerobic methanotrophs in lake sediment.
  25. Noll, M., Frenzel, P., and Conrad, R. (2008) Selective stimulation of type I methanotrophs in a rice paddy soil by urea fertilization revealed by RNA-based stable isotope probing. FEMS Microbiol Ecol 65: 125-132.
  26. Murase, J., and Frenzel, P. (2008) Selective grazing of methanotrophs by protozoa in a rice field soil. FEMS Mircobiol Ecol 65: 408-414.
  27. Siljanen, H.M.P., Saari, A., Krause, S., Lensu, A., Abell, G.C.J., Bodrossy, L., et al. (2011) Hydrology is reflected in the functioning and community composition of methanotrophs in the littoral wetland of a boreal lake. FEMS Microbiol Ecol 75: 430- 445.
  28. Prior,S.D. and Dalton,H. (1985) Acetylene as a suicide substrate and active site probe for monooxygenase from Methylococcus capsulatus (Bath). FEMS Microbiol. Lett. 29: 105- 109.
  29. Kumaresan, D., Stralis-Pavese, N., Abell, G.C.J., Bodrossy, L., and Murrell, J.C. (2011) Physical disturbance to ecological niches created by soil structure alters community composition of methanotrophs. Environ Microbiol Rep 3: 613-621.
  30. McDonald, I.R., Bodrossy, L., Chen, Y., and Murrell, C. (2008) Molecular ecology techniques for the study of aerobic methanotrophs. Appl Environ Microbiol 74: 1305- 1315.
  31. Kip, N., Ouyang, W., van Winden, J., Raghoebarsing, A., van Niftrik, L., Pol, A., et al. (2011) Detection, isolation, and characterization of acidophilic methanotrophs from Sphagnum mosses. Appl Environ Microbiol 77: 5643-5654.
  32. Knief, C., Lipski, A., and Dunfield, P. (2003) Diversity and activity of methanotrophic bacteria in different upland soils. Appl Environ Microbiol 69: 6703-6714.
  33. Mohanty, S.R., Bodelier, P.L.E., Floris, V., and Conrad, R. (2006) Differential effects of nitrogenous fertilizers on methane-consuming microbes in rice field and forest soils. Appl Environ Microbiol 72: 1346-1354.
  34. Svenning, M.M., Hestnes, A.G., Wartiainen, I., Stein, L.Y., Klotz, M.G., Kalyuzhnaya, M.G., et al. (2011) Genome sequence of the Artic methanotroph Methylobacter tundripaludum SV96. J Bacteriol 193: 6418-6419.
  35. Trotsenko, Y.A., Medvedkova, K.A., Khmelenina, V.N., and Eshinimayev, B.T. (2009) Thermophilic and thermotolerant aerobic methanotrophs. Microbiol 78: 387-401.
  36. Vorobev, A.V., Baani, M., Doronina, N.V., Brady, A.L., Liesack, W., Dunfield, P.F., and Dedysh, S.V. (2011) Methyloferula stellata gen. nov., sp. nov., an acidophilic, obligately methanotrophic bacterium that possesses only a soluble methane monooxygenase. Int J Syst Evol Microbiol 61: 2456-2463.
  37. Stanley, S.H., Prior, S.D., Leak, D.J., and Dalton, H. (1983) Copper stress underlies the fundamental change in intracellular location of methane mono-oxygenase in methane- oxidizing organisms: studies in batch and continuous cultures. Biotechnol Lett 5: 487- 492.
  38. Liebner, S., Rublack, K., Stuehrmann, T., and Wagner, D. (2009) Diversity of aerobic methanotrophic bacteria in a permafrost active layer soil of the Lena Delta, Siberia. Microbiol Ecol 57: 25-35.
  39. Tavormina,P.L., Orphan,V.J., Kalyuzhnaya,M.G., Jetten,M.S.M., and Klotz,M.G. (2011) A novel family of functional operons encoding methane/ammonia monooxygenase- related proteins in gammaproteobacterial methanotrophs. Environ. Microbiol. Rep. 3: 91-100.
  40. Strous, M. (2011) Beyond denitrification: alternative routes to dinitrogen. In Moir, J.W.B. (eds). Nitrogen Cycling in Bacteria: Molecular analysis. Caister Academic Press: Norfolk, UK, pp 123-133.
  41. Bodelier,P.L.E. and Frenzel,P. (1999) Contribution of methanotrophic and nitrifying bacteria to CH4 and NH4+ oxidation in the rice rhizosphere using new methods for discrimination. Appl. Environ. Microbiol. 65: 1826-1833.
  42. Andreas Reim and Peter Frenzel; " COUNTER-GRADIENTS OF METHANE AND OXYGEN – How methanotrophs shape their environment and limit their own activity " ; ISME 13 th Spatial Heterogeneity – Small Volumes with Big Impacts; August 2010; Seattle, USA (Oral presentation)
  43. Andreas Reim and Peter Frenzel; " Effect of energy flow on the susceptibility of aerobic methanotrophic communities to disturbance " ; GRC: Molecular Basis of Microbial One- Carbon Metabolism; August 2012; Lewiston ME, USA, (Poster presentation)
  44. Nyerges, G., Han, S., and Stein, L.Y. (2010) Effects of ammonium and nitrite on growth and competitive fitness of cultivated methanotrophic bacteria. Appl Environ Microbiol 76: 5648-5651.
  45. Andreas Reim; " Effects of energy flow on diversity, resistance and resilience of methanotrophs " ; 2 nd MECOMECON Project Meeting; April 2011; Tromsø, Norway (Oral presentation)
  46. Op den Camp, H.J.M., Islam, T., Stott, M.B., Harhangi, H.R., Hynes, A., Schouten, S., Jetten, M.S.M., et al. (2009) Environmental, genomic and taxonomical perspectives on methanotrophic Verrucomicrobia. Environ Microbiol Rep 1: 293-306.
  47. Graham,D.W., Chaudhary,J.A., Hanson,R.S., and Arnold,R.G. (1993) Factors affecting competition between type-I and type-II methanotrophs in 2-organism, continuous- flow reactors. Microb. Ecol. 25: 1-17.
  48. Stein, L.Y., Bringel, F., DiSpirito, A.A., Han, S., Jetten, M.S.M., Kalyuzhnaya, M.G., et al., (2011) Genome sequence of the methanotrophic Alphaproteobacterium Methylocystis sp. Strain Rockwell (ATCC 49242). J Bacteriol 193: 2668-2669.
  49. Stein, L.Y., Yoon, S., Semrau, J.D., DiSpirito, A.A., Crombie, A., Murrell, J.C., et al. (2010) Genome sequence of the obligate methanotroph Methylosinus trichosporium Strain OB3b. J Bacteriol 192: 6497-6498.
  50. Ward, N., Larsen, O., Sakwa, J., Bruseth, L., Khouri, H., Durkin, A.S., et al. (2004) Genomic insights into methanotrophy: The complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2: 1616-1628.
  51. Amaral,J.A. and Knowles,R. (1995) Growth of methanotrophs in methane and oxygen counter gradients. FEMS Microbiol. Lett. 126: 215-220.
  52. Andreas Reim and Peter Frenzel; " Half a millimeter makes a difference: a microscale study on distribution and specific activity of methanotrophs at an oxic-anoxic interface " ; VAAM annual conference Environmental Microbiology; April, 2011; Karlsruhe, Germany (Oral presentation)
  53. Schnell, S., and King, G. (1994) Mechanistic analysis of ammonium inhibition of atmospheric methane consumption in forest soils. Appl Environ Microbiol 60: 3514- 3521.
  54. Krause,S., Lüke,C., and Frenzel,P. (2012) Methane source strength and energy flow shape methanotrophic communities in oxygen methane counter-gradients. Environ. Microbiol. Rep. 4: 203-208.
  55. Lennon,J.T. and Jones,S.E. (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Micro 9: 119-130.
  56. Lee, S-W., Keeney, D.R., Lim, D-H., Dispirito, A.A., and Semrau, J.D. (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.
  57. Lüke,C. Molecular ecology and biogeography of methanotrophic bacteria in wetland rice fields. 2010. PhD Thesis
  58. Murrell, J.C., and Dalton, H. (1983) Nitrogen fixation in obligate methanotrophs. Microbiol 129: 3481-3486.
  59. Reim,A., Lüke,C., Krause,S., Pratscher,J., and Frenzel,P. (2012) One millimetre makes the difference: high-resolution analysis of methane-oxidizing bacteria and their specific activity at the oxic-anoxic interface in a flooded paddy soil. ISME. J. 6: 2128-2139.
  60. Semrau, J.D., Chistoserdov, A., Lebron, J. Costello, A., Davagnino, J., Kenna, E., et al. (1995) Particulate methane monooxygenase genes in methanotrophs. J Bacteriol 177: 3071-3079.
  61. Reim,A., and Frenzel,P Effect of energy flow on the susceptibility of aerobic methanotroph communities to disturbance. In preparation.
  62. Pieja, A.J., Sundstrom, E.R., and Criddle, C.S. (2011) Poly-3-hydroxybutyrate metabolism in the type II methanotroph Methylocystis parvus OBBP. Appl Environ Microbiol 77: 6012-6019.
  63. Collet,S., Reim,A., and Frenzel,P Recovery of paddy soil methanotrophs from drought. In preparation.
  64. Salehizadeh, H., and Van Loosdrecht, M.C.M. (2004) Production of polyhydroxyalkanoate by mixed culture: recent trends and biotechnological importance. Biotechnol Adv 22: 261-279.
  65. Kolb, S., Knief, C., Stubner, S., and Conrad, R. (2003) Quantitative detection of methanotrophs in soils by novel pmoA-targeted real-time PCR assays. Appl Environ Microbiol 69: 2423-2429.
  66. Ho,A., Lüke,C., and Frenzel,P. (2011b) Recovery of methanotrophs from disturbance: population dynamics, evenness and functioning. ISME. J. 5: 750-758.
  67. Murrell, J.C., McDonald, I.R., and Gilbert, B. (2000) Regulation of expression of methane monooxygenases by copper ions. Trends Microbiol 8: 221-225.
  68. Allison,S.D. and Martiny,J.B.H. (2008) Resistance, resilience, and redundancy in microbial References Krüger,M., Frenzel,P., and Conrad,R. (2001) Microbial processes influencing methane References Wertz,S., Degrange,V., Prosser,J.I., Poly,F., Commeaux,C., Freitag,T. et al. (2006) Maintenance of soil functioning following erosion of microbial diversity. Environ. Microbiol. 8: 2162-2169.
  69. Wang,Z., Gerstein,M., and Snyder,M. (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63.
  70. Andrews JH & Harris RF (1986) R-selection and K-selection and microbial ecology. Adv Microb Ecol 9: 99–147.
  71. Pfluger, A.R., Wu, W., Pieja, A.J., Wan, J., Rostkowski, K.H., and Criddle., C.S. (2011) Selection of type I and type II methanotrophic proteobacteria in a fluidized bed reactor under non-sterile conditions. Bioresource Technol 102: 9919-9926.
  72. Krause S, Lüke C, Frenzel P. (2009). Spatial heterogeneity of methanotrophs: a geostatistical analysis of pmoA-based T-RFLP patterns in a paddy soil. Environ Microbiol Rep 1: 393-397
  73. Radajewski,S., Ineson,P., Parekh,N.R., and Murrell,C. (2000) Stable isotope probing as a tool in microbial ecology. Nature 403: 646-649.
  74. Krause, S., Lüke, C., and Frenzel, P. (2010) Succession of methanotrophs in oxygen- methane counter-gradients of flooded rice paddies. ISME J 4: 1603-1607.
  75. MacArthur, R.H. and Wilson, E.O. (1967) The theory of island biogeography, 13 th edn. Princeton, UK: Princeton University Press.
  76. Yimga, M.T., Dunfield, P.F., Ricke, P., Heyer, J., and 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.
  77. Whittenbury, R., Davies, S.L., and Davey, J.F. (1970) Exospores and cysts formed by methane-utilizing bacteria. J General Microbiol 61: 219-226.
  78. Orcutt, B.N., Sylvan, J.B., Knab, N.J., and Edwards, K.J. (2011) Microbial ecology of the dark ocean above, at, and below the seafloor. Microbiol Mol Biol Rev 75: 361-422.
  79. Chen,Y., Dumont,M.G., Cebron,A., and Murrell,J.C. (2007) Identification of active methanotrophs in a landfill cover soil through detection of expression of 16S rRNA and functional genes. Environ. Microbiol. 9: 2855-2869.
  80. Chen,Y., Dumont,M.G., McNamara,N.P., Chamberlain,P.M., Bodrossy,L., Stralis-Pavese,N., and Murrell,J.C. (2008) Diversity of the active methanotrophic community in acidic peatlands as assessed by mRNA and SIP-PLFA analyses. Environ. Microbiol. 10: 446- 459.
  81. Lüke, C., Krause, S., Cavigiolo, S., Greppi, D., Lupotto, E., and Frenzel, P. (2010) Biogeography of wetland rice methanotrophs. Environ Microbiol 12: 862-872.
  82. Kolb, S. (2009) The quest for atmospheric methane oxidizers in forest soils. Environ Microbiol Rep 1: 336-346.
  83. Lüke, C., Bodrossy, L., Lupotto, E., and Frenzel, P. (2011) Methanotrophic bacteria associated to rice roots: the cultivar effect assessed by T-RFLP and microarray analysis. Environ Microbiol Rep 3: 518-525.
  84. Ho,A., Lüke,C., Cao,Z., and Frenzel,P. (2011a) Ageing well: methane oxidation and methane oxidizing bacteria along a chronosequence of 2000 years. Environ. Microbiol. Rep. 3: 738-743.
  85. Micheli,F., Cottingham,K.L., Bascompte,J., Bjørnstad,O.N., Eckert,G.L., Fischer,J.M. et al. (1999) The Dual Nature of Community Variability. Oikos 85: 161-169.
  86. Qiu, Q., Noll, M., Abraham, R., Lu, Y., and Conrad, R. (2008) Applying stable isotope probing of phospholipid fatty acids and rRNA in a Chinese rice field to study activity and composition of the methanotrophic bacterial communities in situ. ISME J 2: 602- 614.
  87. Levine, U.Y., Teal, T.K., Robertson, G.P., and Schmidt, T.M. (2011) Agriculture's impact on microbial diversity and associated fluxes of carbon dioxide and methane. ISME J 5: 1683-1691.
  88. Pol,A., Heijmans,K., Harhangi,H.R., Tedesco,D., Jetten,M.S.M., and Op den Camp,H.J.M. (2007) Methanotrophy below pH1 by a new Verrucomicrobia species. Nature 450: 874- 878.
  89. Kip, N., van Winden, J.F., Pan, Y., Bodrossy, L., Reichart, G., Smolders, A.J.P., et al. (2010) Global prevalence of methane oxidation by symbiotic bacteria in peat-moss ecosystems. Nature Geosci 3: 617-621.
  90. Baani,M. and Liesack,W. (2008) Two isozymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp strain SC2. PNAS 105: 10203-10208.
  91. Eller,G., Krüger,M., and Frenzel,P. (2005) Comparing field and microcosm experiments: a case study on methano-and methylotrophic bacteria in paddy soil. FEMS Microbiol. Ecol. 51: 279-291.


* Das Dokument ist im Internet frei zugänglich - Hinweise zu den Nutzungsrechten