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.
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References
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.
Ariya, P. A., Nepotchatykh, O., Ignatova, O., & Amyot, M. (2002). Microbiological degradation of atmospheric organic compounds. Geophysical Research Letters, 29(22), 2077–2081.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.
Felsenstein, J. (1993). Phylogeny inference package (PHYLIP) version 3.5. Seattle: University of Washington.
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.
Hanson, R. S., & Hanson, T. E. (1996). Methanotrophic Bacteria. Microbiological Reviews, 60(2), 439–471.
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.
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.
Jensen, S., Priemé, A., & Bakken, L. (1998). Methanol improves methane uptake in starved methanotrophic microorganisms. Applied and Environmental Microbiology, 64(3), 1143–1146.
Knief, C., & Dunfield, P. F. (2005). Response and adaptation of different methanotrophic bacteria to low methane mixing ratios. Environmental Microbiology, 7(9), 1307–1317.
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.
Kvenvolden, K. A., & Rogers, B. W. (2005). Gaia’s breath—global methane exhalations. Marine and Petroleum Geology, 22, 579–590.
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.
Pfennig, N. (1962). Beobachtungen über das Schwärmen von Chromatium okenii. Archives of Microbiology, 42(1), 90–95.
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.
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.
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.
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.
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.
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.
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.
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.
West, A. E., & Schmidt, S. K. (1999). Acetate stimulates atmospheric CH4 oxidation by an alpine tundra soil. Soil Biology & Biochemistry, 31(12), 1649–1655.
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.
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.
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.
Wuebbles, D. J., & Hayhoe, K. (2002). Atmospheric methane and global change. Earth-Science Reviews, 57, 177–210.
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.
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.
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.
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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
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DOI: https://doi.org/10.1007/s10453-013-9287-1