Viable methanotrophic bacteria enriched from air and rain can oxidize methane at cloud-like conditions

Abstract

Atmospheric methane is degraded by both photooxidation and, in topsoils, by methanotrophic bacteria, but this may not totally account for the global sink of this greenhouse gas. Topsoils are a prominent source of airborne bacteria, which can degrade some organic atmospheric compounds at rates similar to photooxidation. Although airborne methanotrophs would have direct access to atmospheric methane, their presence and activity in the atmosphere has not been investigated so far. We enriched airborne methanotrophs from air and rainwater and showed that they oxidized methane at atmospheric concentration. The majority of seven OTUs, detected using pmoA gene clone libraries, were affiliated to the type II methanotrophic genera Methylocystis and Methylosinus. Furthermore, 16S rRNA gene clone libraries revealed the presence of OTUs affiliated with the genera Hyphomicrobium and Variovorax, members of which can stimulate methane oxidation by yet unidentified mechanisms. Simulating cloud-like conditions revealed that although both low pH and the presence of common cloud-borne organics negatively affected methane oxidation, airborne methanotrophs were able to degrade atmospheric methane in most cases. We demonstrate here for the first time that viable methanotrophic bacteria are present in air and rain and thus expand our knowledge on the global distribution of methanotrophs to include the atmosphere. The fact that they can degrade methane to below atmospheric concentrations when inoculated into artificial cloud water leads to an important possible effect of these organisms: the atmosphere may not only function as a medium for microbial dissemination, but also as a site of active microbial methane turnover.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Amato, P., Menager, M., Sancelme, M., Laj, P., Mailhot, G., & Delort, A. M. (2005). Microbial population in cloud water at the Puy de Dome: Implications for the chemistry of clouds. Atmospheric Environment, 39(22), 4143–4153.

    Article  CAS  Google Scholar 

  2. Ariya, P. A., Nepotchatykh, O., Ignatova, O., & Amyot, M. (2002). Microbiological degradation of atmospheric organic compounds. Geophysical Research Letters, 29(22), 2077–2081.

    Article  Google Scholar 

  3. Baani, M., & Liesack, W. (2007) Two isozymes of particulate methane monooxygenase with different methane oxidation kinetics are found in Methylocystis sp. strain SC2. Proceedings of the National Academy of Sciences, 105(29), 10203–10208.

    Google Scholar 

  4. Bárcena, T., Yde, J. C., & Finster, K. W. (2010). Methane flux and high-affinity methanotrophic diversity along the chronosequence of a receding glacier in Greenland. Annals of Glaciology, 51(56), 23–31.

    Article  Google Scholar 

  5. Blando, J. D., & Turpin, B. J. (2000). Secondary organic aerosol formation in cloud and fog droplets: A literature evaluation of plausibility. Atmospheric Environment, 34, 1623–1632.

    Article  CAS  Google Scholar 

  6. Bull, I. D., Parekh, N. R., Hall, G. H., Ineson, P., & Evershed, R. P. (2000). Detection and classification of atmospheric methane oxidizing bacteria in soil. Nature, 405, 175–178.

    Article  CAS  Google Scholar 

  7. Burrows, S. M., Elbert, W., Lawrence, M. G., & Pöschl, U. (2009). Bacteria in the global atmosphere—Part 1: Review and synthesis of literature data for different ecosystems. Atmospheric Chemistry and Physics Discussions, 9, 10777–10827.

    Article  Google Scholar 

  8. Christophersen, M., Linderød, L., Jensen, P. E., & Kjeldsen, P. (2000). Methane oxidation at low temperatures in soil exposed to landfill gas. Journal of Environmental Quality, 29, 1989–1997.

    Article  CAS  Google Scholar 

  9. Degelmann, D. M., Borken, W., Drake, H. L., & Kolb, S. (2010). Different atmospheric methane-oxidizing communities in European beech and Norway spruce soils. Applied and Environmental Microbiology, 76(10), 3228–3235.

    Article  CAS  Google Scholar 

  10. Dunfield, P. F., Liesack, W., Henckel, T., Knowles, R., & Conrad, R. (1999). High-affinity methane oxidation by a soil enrichment culture containing a type II methanotroph. Applied and Environmental Microbiology, 66(9), 4136–4138.

    Article  Google Scholar 

  11. Dunfield, P. F., Yimga, M. T., Dedysh, S. N., Berger, U., Liesack, W., & Heyer, J. (2002). Isolation of a Methylocystis strain containing a novel pmoA-like gene. FEMS Microbiology Ecology, 41, 17–26.

    Article  CAS  Google Scholar 

  12. Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

    Article  CAS  Google Scholar 

  13. Felsenstein, J. (1993). Phylogeny inference package (PHYLIP) version 3.5. Seattle: University of Washington.

    Google Scholar 

  14. Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  15. Hanson, R. S., & Hanson, T. E. (1996). Methanotrophic Bacteria. Microbiological Reviews, 60(2), 439–471.

    CAS  Google Scholar 

  16. Hueglin, C., Gehrig, R., Baltensperger, U., Gysel, M., Monn, C., & Vonmont, H. (2004). Chemical characterisation of PM2.5, PM10 and coarse particles at urban, near-city and rural sites in Switzerland. Atmospheric Environment, 39(4), 637–651.

    Article  Google Scholar 

  17. Isaksen, I. S. A., Granier, C., Myhre, G., Berntsen, T. K., Dalsøren, S. B., Gauss, M., et al. (2009). Atmospheric composition change: Climate–Chemistry interactions. Atmospheric Environment, 43, 5138–5192.

    Article  CAS  Google Scholar 

  18. Jensen, S., Priemé, A., & Bakken, L. (1998). Methanol improves methane uptake in starved methanotrophic microorganisms. Applied and Environmental Microbiology, 64(3), 1143–1146.

    CAS  Google Scholar 

  19. Knief, C., & Dunfield, P. F. (2005). Response and adaptation of different methanotrophic bacteria to low methane mixing ratios. Environmental Microbiology, 7(9), 1307–1317.

    Article  CAS  Google Scholar 

  20. Knief, C., Lipski, A., & Dunfield, P. F. (2003). Diversity and activity of methanotrophic bacteria in different upland soils. Applied and Environmental Microbiology, 69(11), 6703–6714.

    Article  CAS  Google Scholar 

  21. Kvenvolden, K. A., & Rogers, B. W. (2005). Gaia’s breath—global methane exhalations. Marine and Petroleum Geology, 22, 579–590.

    Article  CAS  Google Scholar 

  22. Marinoni, A., Laj, P., Sellegri, K., & Mailhot, G. (2004). Cloud chemistry at the Puy de Dôme: Variability and relationships with environmental factors. Atmospheric Chemistry and Physics, 4, 715–728.

    Article  CAS  Google Scholar 

  23. Pfennig, N. (1962). Beobachtungen über das Schwärmen von Chromatium okenii. Archives of Microbiology, 42(1), 90–95.

    CAS  Google Scholar 

  24. Ricke, P., Kolb, S., & Braker, G. (2005). Application of a newly developed ARB software-integrated tool for in Silico terminal restriction fragment length polymorphism analysis reveals the dominance of a novel pmo a cluster in a forest soil. Applied and Environmental Microbiology, 71(3), 1671–1673.

    Article  CAS  Google Scholar 

  25. Schloss, P. D., & Handelsman, J. (2005). Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied and Environmental Microbiology, 71, 1501–1506.

    Article  CAS  Google Scholar 

  26. Staley, J. T., Brenner, D. J., & Krieg, N. R. (2005). Volume two: The proteobacteria. In G. M. Garrity (Ed.), Bergey’s manual of systematic bacteriology (2nd ed., pp. 411–476). Berlin: Springer.

    Google Scholar 

  27. Svenning, M. M., Wartiainen, I., Hestnes, A. G., & Binnerup, S. J. (2003). Isolation of methane oxidising bacteria from soil by use of a soil substrate membrane system. FEMS Microbiology Ecology, 44, 347–354.

    Article  CAS  Google Scholar 

  28. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731–2739.

    Article  CAS  Google Scholar 

  29. Temkiv, T. Š., Finster, K., Hansen, B. M., Nielsen, N. W., & Karlson, U. G. (2012). The microbial diversity of a storm cloud as assessed by hailstones. FEMS Microbiology Ecology, 81(3), 684–695.

    Article  CAS  Google Scholar 

  30. Vaïtilingom, M., Amato, P., Sancelme, M., Laj, P., Leriche, M., & Delort, A. M. (2010). Contribution of microbial activity to carbon chemistry in clouds. Applied and Environmental Microbiology, 76(1), 23–29.

    Article  Google Scholar 

  31. Wang, J. S., McElroy, M. B., Logan, J. A., Palmer, P. I., Chameides, W. L., Wang, Y., et al. (2008). A quantitative assessment of uncertainties affecting estimates of global mean OH derived from methyl chloroform observations. Journal of Geophysical Research, 113(D12). doi:10.1029/2007JD008496.

    Google Scholar 

  32. West, A. E., & Schmidt, S. K. (1999). Acetate stimulates atmospheric CH4 oxidation by an alpine tundra soil. Soil Biology & Biochemistry, 31(12), 1649–1655.

    Article  CAS  Google Scholar 

  33. Whittenbury, R., Phillips, K. C., & Wilkinson, J. F. (1970). Enrichment, isolation and some properties of methane-utilizing bacteria. Journal of General Microbiology, 61, 205–218.

    Article  CAS  Google Scholar 

  34. Wilkinson, T. G., & Harrison, D. E. F. (1973). The affinity for methane and methanol of mixed cultures grown on methane in continuous culture. Journal of Applied Bacteriology, 36, 309–313.

    Article  CAS  Google Scholar 

  35. Wise, M. G., McArthur, J. V., & Shimkets, L. J. (1999). Methanotroph diversity in landfill soil: Isolation of novel type I and type II methanotrophs whose presence was suggested by culture-independent 16S ribosomal DNA analysis. Applied and Environmental Microbiology, 65(11), 4887–4897.

    CAS  Google Scholar 

  36. Wuebbles, D. J., & Hayhoe, K. (2002). Atmospheric methane and global change. Earth-Science Reviews, 57, 177–210.

    Article  CAS  Google Scholar 

  37. Yimga, M. T., Dunfield, P. F., 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. Applied and Environmental Microbiology, 69(9), 5593–5602.

    Article  CAS  Google Scholar 

  38. Zweifel, U. L., Hagström, Å., Holmfeldt, K., Thyrhaug, R., Geels, C., Frohn, L. M., et al. (2012). High bacterial 16S rRNA gene diversity above the atmospheric boundary layer. Aerobiologia, 28(4), 481–498. doi:10.1007/s10453-012-9250-6.

    Google Scholar 

Download references

Acknowledgments

T.Š.-T. was supported by a PhD fellowship granted by the Danish Agency for Science, Technology and Innovation (Forsknings- og Innovationsstyrelsen). Funding for the Stellar Astrophysics Centre is provided by The Danish National Research Foundation. The research is supported by the ASTERISK project (ASTERoseismic Investigations with SONG and Kepler) funded by the European Research Council (Grant agreement no.: 267864). The authors thank Lotte Frederiksen, Tove Wiegers and Fariba Barandazi for skilled technical assistance. We gratefully acknowledge the valuable advice of Teresa G. Bárcena and Svend Binnerup.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ulrich Gosewinkel Karlson.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Šantl-Temkiv, T., Finster, K., Hansen, B.M. et al. Viable methanotrophic bacteria enriched from air and rain can oxidize methane at cloud-like conditions. Aerobiologia 29, 373–384 (2013). https://doi.org/10.1007/s10453-013-9287-1

Download citation

Keywords

  • Air microbiology
  • Methane
  • Methanotrophs
  • Methylocystis
  • Aerial dispersal
  • Airborne bacteria