Skip to main content

Advertisement

SpringerLink
Log in

High bacterial 16S rRNA gene diversity above the atmospheric boundary layer

  • Original Paper
  • Published:
Aerobiologia Aims and scope Submit manuscript

Abstract

The atmosphere is host to an omnipresent bacterial community that may influence fundamental atmospheric processes such as cloud formation and precipitation onset. Knowledge of this bacterial community is scarce, particularly in air masses relevant to cloud formation. Using a light aircraft, we sampled above the atmospheric boundary layer—that is, at heights at which cloud condensation occurs—over coastal areas of Sweden and Denmark in summer 2009. Enumeration indicated total bacterial numbers of 4 × 101 to 1.8 × 103 m−3 air and colony-forming units of 0–6 bacteria m−3 air. 16S rRNA gene libraries constructed from samples collected above the Baltic Sea coast revealed a highly diverse bacterial community dominated by species belonging to the genera Sphingomonas and Pseudomonas. Bacterial species known to carry ice-nucleating proteins were found in several samples. Modeled back trajectories suggested the potential sources of the sampled bacteria to be diverse geographic regions, including both marine and terrestrial environments in the northern hemisphere. Several samples contained 16S rRNA genes from plant chloroplasts, confirming a terrestrial contribution to these samples. Interestingly, the airborne bacterial community displayed an apparent seasonal succession that we tentatively ascribe to in situ succession in the atmosphere.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403–410.

    CAS  Google Scholar 

  • Amato, P., Parazols, M., Sancelme, M., Laj, P., Mailhot, G., & Delort, A. M. (2007). Microorganisms isolated from the water phase of tropospheric clouds at the puy de dome: Major groups and growth abilities at low temperatures. FEMS Microbiology Ecology, 59(2), 242–254.

    Article  CAS  Google Scholar 

  • Ashelford, K. E., Chuzhanova, N. A., Fry, J. C., Jones, A. J., & Weightman, A. J. (2005). At least one in twenty 16 s rrna sequence records currently held in public repositories estimated to contain substantial anomalies. Applied and Environmental Microbiology, 12, 7724–7736.

    Article  Google Scholar 

  • Balkwill, D. L., Fredrickson, J. K., & Romine, M. F. (2006). Sphingomonas and related genera. In M. Dworkin, S. Falkow, E. Rosenberg, K. H. Schleifer, & E. Stackebrandt (Eds.), The prokaryotes: A handbook on the biology of bacteria (pp. 605–630). Singapore: Springer-Science.

    Google Scholar 

  • Bauer, H., Kasper-Giebl, A., Löflund, M., Giebl, H., Hitzenberger, R., Zibuschka, F., et al. (2002). The contribution of bacteria and fungal spores to the organic carbon content of cloud water, precipitation and aerosols. Atmospheric Research, 64, 109–119.

    Article  CAS  Google Scholar 

  • Bowers, R. M., Lauber, C. L., Wiedinmyer, C., Hamady, M., Hallar, A. G., Fall, R., et al. (2009). Characterization of airborne microbial communities at a high-elevation site and their potential to act as atmospheric ice nuclei. Applied and Environmental Microbiology, 75, 5121–5130.

    Article  CAS  Google Scholar 

  • Brandt, J., Christensen, J. H., Frohn, L. M., & Berkowicz, R. (2001a). Operational air pollution forecasts from regional scale to urban street scale. Part 1: System description. Physics and Chemistry of the Earth Part B-Hydrology Oceans and Atmosphere, 26, 781–786.

    Article  Google Scholar 

  • Brandt, J., Christensen, J. H., Frohn, L. M., & Berkowicz, R. (2001b). Operational air pollution forecasts from regional scale to urban street scale. Part 2: Performance evaluation Physics and Chemistry of the Earth Part B-Hydrology Oceans and Atmosphere, 26, 825–830.

  • Brodie, E. L., DeSantis, T. Z., Parker, J. P. M., Zubietta, I. X., Piceno, Y. M., & Andersen, G. L. (2007). Urban aerosols harbor diverse and dynamic bacterial populations. Proceedings of the National Academy of Sciences, USA, 104(1), 299–304.

    Article  CAS  Google Scholar 

  • Cho, B. C., & Hwang, C. Y. (2011). Prokaryotic abundance and 16 s rrna gene sequences detected in marine aerosols on the east sea (korea). FEMS Microbiology Ecology, 76, 327–341.

    Article  CAS  Google Scholar 

  • Christner, B. C., Cai, R., Morris, C. E., McCarter, K. S., Foreman, C. M., Skidmore, M. L., et al. (2008a). Geographic, seasonal, and precipitation chemistry influence on the abundance and activity of biological ice nucleators in rain and snow. Proceedings of the National Academy of Sciences, USA, 105, 18854–18859.

    Article  CAS  Google Scholar 

  • Christner, B. C., Morris, C. E., Foreman, C. M., Cai, R., & Sands, D. C. (2008b). Ubiquity of biological ice nucleators in snowfall. Science, 319, 1214–1214.

    Article  CAS  Google Scholar 

  • Despres, V., Nowoisky, J., Klose, M., Conrad, R., Andreae, M. O., & Pöschl, U. (2007). Molecular genetics and diversity of primary biogenic aerosol particles in urban, rural, and high alpine air. Biogeosciences Discussions, 4, 349–384.

    Article  Google Scholar 

  • Di Giorgio, C., Krempff, A., Guiraud, H., Binder, P., Tiret, C., & Dumenil, G. (1996). Atmospheric pollution by airborne microorganisms in the city of marseilles. Atmospheric Environment, 30(1), 155–160.

    Article  Google Scholar 

  • Draxler, R. R., & Rolph, G. D. (2010). Hybrid single-particle lagrangian integrated trajectory (hysplit). Model access via noaa arl ready website: http://ready.Arl.Noaa.Gov/hysplit.Php.

  • Du, H. L., Jiao, N. Z., Hu, Y. H., & Zeng, Y. H. (2006). Diversity and distribution of pigmented heterotrophic bacteria in marine environments. FEMS Microbiology Ecology, 57, 92–105.

    Article  CAS  Google Scholar 

  • Fahlgren, C., Bratbak, G., Sandaa, R.-A., Thyrhaug, R., & Zweifel, U. L. (2011). Diversity of airborne bacteria in samples collected using different devices for aerosol collection. Aerobiologia, 27, 107–120.

    Article  Google Scholar 

  • Fahlgren, C., Hagström, Å., Nilsson, D., & Zweifel, U. L. (2010). Annual variations in the diversity, viability, and origin of airborne bacteria. Applied and Environmental Microbiology, 76, 3015–3025.

    Article  CAS  Google Scholar 

  • Fang, Z., Ouyang, Z., Zheng, H., Wang, X., & Hu, L. (2007). Culturable airborne bacteria in outdoor environments in beijing, china. Microbial Ecology, 54(3), 487–496.

    Article  Google Scholar 

  • Fierer, N., Liu, Z. Z., Rodriguez-Hernandez, M., Knight, R., Henn, M., & Hernandez, M. T. (2008). Short-term temporal variability in airborne bacterial and fungal populations. Applied and Environmental Microbiology, 74(1), 200–207.

    Article  CAS  Google Scholar 

  • Franc, G. D., & DeMott, P. J. (1998). Cloud activation characteristics of airborne erwinia carotovora cells. Journal of Applied Meteorology, 37, 1293–1300.

    Article  Google Scholar 

  • González, A. J., & Rodicio, R. (2007). Erwinia persicina causing chlorosis and necrotic spots in leaves and tendrils of pisum sativum in southeastern spain. Plant Disease, 91, 460.

    Article  Google Scholar 

  • Griffin, D. W., Kellogg, C. A., Garrison, V. H., Lisle, J. T., Borden, T. C., & Shinn, E. A. (2003). Atmospheric microbiology in the northern Caribbean during African dust events. Aerobiologia, 19, 143–157.

    Article  Google Scholar 

  • Hertel, O., Skjøth, C. A., Brandt, J., Christensen, J. H., Frohn, L. M., & Frydendall, J. (2003). Operational mapping of atmospheric nitrogen deposition to the Baltic Sea. Atmospheric Chemistry and Physics, 3, 2083–2099.

    Article  CAS  Google Scholar 

  • Hertel, O., Skjøth, C. A., & Fenger, J. (2009). Atmospheric physics, chapter 9. In J. Fenger, & J. C. Tjell (Eds.), Air pollution—From a local to a global perspective (p. 488). Polyteknisk forlag.

  • Hervàs, A., Camarero, L., Reche, I., & Casamayor, E. O. (2009). Viability and potential for immigration of airborne bacteria from Africa that reach high mountain lakes in Europe. Environmental Microbiology, 11, 1612–1623.

    Article  Google Scholar 

  • Hervàs, A., & Casamayor, E. O. (2009). High similarity between bacterioneuston and airborne bacterial community compositions in a high mountain lake area. FEMS Microbiology Ecology, 67, 219–228.

    Article  Google Scholar 

  • Holm, E., & Jensen, V. (1972). Aerobic chemoorganotrophic bacteria of a Danish beech forest. OIKOS, 23, 248–260.

    Article  Google Scholar 

  • Huber, T., Faulkner, G., & Hugenholtz, P. (2004). Bellerophon: A program to detect chimeric sequences in multiple sequence alignments. Bioinformatics, 20, 2317–2319.

    Article  CAS  Google Scholar 

  • Janjic, Z. I. (1990). The step-mountain coordinate: Physical package. Monthly Weather Review, 118, 1429–1443.

    Article  Google Scholar 

  • Janjic, Z. I. (1994). The step-mountain eta coordinate model: Further developments of the convection, viscous sublayer, and turbulence closure schemes. Monthly Weather Review, 122, 927–945.

    Article  Google Scholar 

  • Janssen, P. H. (2006). Identifying the dominant soil bacterial taxa in libraries of 16 s rrna and 16 s rrna genes. Applied and Environmental Microbiology, 72, 1719–1728.

    Article  CAS  Google Scholar 

  • Kaarakainen, P., Meklin, T., Rintala, H., Hyvärinen, A., Kärkkäinen, P., Vepsäläinen, A., et al. (2008). Seasonal variation in airborne microbial concentrations and diversity at landfill, urban and rural sites. CLEAN - Soil, Air, Water, 36(7), 556–563.

    Article  CAS  Google Scholar 

  • Kasprzyk, I., Myszkowska, D., Grewling, L., Stach, A., Sáikoparija, B., Skjøth, C. A., et al. (2011). The occurrence of ambrosia pollen in rzeszow, krakow and poznan poland: Investigation of trends and possible transport of ambrosia pollen from ukraine. International Journal of Biometeorology, 55, 633–644.

    Article  Google Scholar 

  • Kawahara, H. (2002). The structures and functions of ice crystal-controlling proteins from bacteria. Journal of Bioscience and Bioengineering, 94, 492–496.

    CAS  Google Scholar 

  • Kellogg, C. A., & Griffin, D. W. (2006). Aerobiology and the global transport of desert dust. Trends in Ecology & Evolution, 21(11), 638–644.

    Article  Google Scholar 

  • Kobashigawa, Y., Nishimiya, Y., Miura, K., Ohgiya, S., Miura, A., & Tsuda, S. (2005). A part of ice nucleation protein exhibits the ice-building ability. FEBS Letters, 579, 1493–1497.

    Article  CAS  Google Scholar 

  • Lighthart, B. (1997). The ecology of bacteria in the alfresco atmosphere. FEMS Microbiology Ecology, 23, 263–274.

    Article  CAS  Google Scholar 

  • Lipson, D. A., & Schmidt, S. K. (2004). Seasonal changes in an alpine soil bacterial community in the Colorado Rocky mountains. Applied and Environmental Microbiology, 70, 2867–2879.

    Article  CAS  Google Scholar 

  • Ludwig, W., Strunk, O., Westram, R., Richer, L., Meier, H., Kumar, Y., et al. (2004). Arb: A software environment for sequence data. Nucleic Acids Research, 32, 1363–1371.

    Article  CAS  Google Scholar 

  • Mancinelli, R. L., & Shulls, W. A. (1978). Airborne bacteria in an urban-environment. Applied and Environmental Microbiology, 35(6), 1095–1101.

    CAS  Google Scholar 

  • Maron, P. A., Lejon, D. P. H., Carvalho, E., Bizet, K., Lemanceau, P., Ranjard, L., et al. (2005). Assessing genetic structure and diversity of airborne bacterial communities by DNA fingerprinting and 16 s rdna clone library. Atmospheric Environment, 39(20), 3687–3695.

    Article  CAS  Google Scholar 

  • Martin, G. M., Johnson, D. W., Jonas, P. R., Rogers, D. P., Brooks, I. M., & Barlow, R. W. (1997). Effects of airmass type on the interaction between warm stratocumulus and underlying cumulus clouds in the marine boundary-layer. The Quarterly Journal of the Royal Meteorological Society, 123, 849–882.

    Article  Google Scholar 

  • Möhler, O., DeMott, P. J., Vali, G., & Levin, Z. (2007). Microbiology and atmospheric processes: The role of biological particles in cloud physics. Biogeosciences, 4, 1059–1071.

    Article  Google Scholar 

  • Muryoi, N., Matsukawa, K., Yamade, K., Kawahara, H., & Obata, H. (2003). Purification and properties of an ice-nucleating protein from an ice-nucleating bacterium, pantoea ananatis kuin-3. Journal of Bioscience and Bioengineering, 95, 157–163.

    CAS  Google Scholar 

  • Nejad, P., Ramstedt, M., Granhall, U., Roos, S., & McIvor, I. (2006). Biochemical characterization and identification of ice-nucleation-active (ina) willow pathogens by means of biolog microplate, ina gene primers and pcr-based 16 s rrna-gene analyses. Journal of Plant Diseases and Protection, 113, 97–106.

    CAS  Google Scholar 

  • Pinhassi, J., & Hagström, Å. (2000). Seasonal succession in marine bacterioplankton. Aquatic Microbial Ecology, 21, 245–256.

    Article  Google Scholar 

  • Pinhassi, J., Zweifel, U. L., & Hagström, Å. (1997). Dominant marine bacterioplankton species found among colony-forming bacteria. Applied and Environmental Microbiology, 63, 3359–3366.

    CAS  Google Scholar 

  • Porter, K. G., & Feig, Y. S. (1980). The use of dapi for identifying and counting aquatic microflora. Limnology and Oceanography, 25(5), 943–948.

    Article  Google Scholar 

  • Pruppacher, H. R., & Klett, J. D. (1997). Microphysics of clouds and precipitation (2nd ed.). Dordrecht: Kluwer.

    Google Scholar 

  • Reche, I., Ortega-Retuerta, E., Romera, O., Pulido-Villena, E., Morales-Baquero, R., & Casamayor, E. O. (2009). Effect of Saharan dust inputs on bacterial activity and community composition in mediterranean lakes and reservoirs. Limnology and Oceanography, 54, 869–879.

    Article  CAS  Google Scholar 

  • Sattler, B., Puxbaum, H., & Psenner, R. (2001). Bacterial growth in supercooled cloud droplets. Geophysical Research Letters, 28, 239–242.

    Article  Google Scholar 

  • Schlegel, H. G., & Jannasch, H. W. (1991). Prokaryotes and their habitats. In A. Balows, K. H. Schleifer, H. G. Truper, & M. Dworkin (Eds.), The prokaryotes: A handbook on the biology of bacteria: Ecophysiology, isolation, identification, applications (pp. 90–91). New York: Springer.

    Google Scholar 

  • Seinfeld, J. H., & Pandis, S. N. (1998). Atmospheric chemistry and physics: Chap. 14 New York, USA: Wiley.

  • Shaffer, B. T., & Lighthart, B. (1996). Survey of culturable airborne bacteria at four diverse locations in Oregon: Urban, rural, forest and coastal. Microbial Ecology, 34, 167–177.

    Article  Google Scholar 

  • Sikoparija, B., Smith, M., Skjøth, C. A., Radisic, P., Milkovska, S., Simic, S., et al. (2009). The Pannonian plain as a source of ambrosia pollen in the balkans. International Journal of Biometeorology, 53, 263–272.

    Article  CAS  Google Scholar 

  • Simu, K., Holmfeldt, K., Zweifel, U. L., & Hagstrom, Å. (2005). Culturability and coexistence of colony-forming and single-cell marine bacterioplankton. Applied and Environmental Microbiology, 71(8), 4793–4800.

    Article  CAS  Google Scholar 

  • Singer, C. E., & Ames, B. N. (1970). Sunlight ultraviolet and bacterial DNA base ratios. Science, 170, 822–826.

    Article  CAS  Google Scholar 

  • Skjøth, C. A., Hertel, O., & Ellermann, T. (2002). Use of the acdep trajectory model in the Danish nation-wide background monitoring programme. Physics and Chemistry of the Earth, 27, 1469–1477.

    Article  Google Scholar 

  • Skjøth, C. A., Sommer, J., Brandt, J., Hvidberg, M., Geels, C., Hansen, K., et al. (2008). Copenhagen—A significant source of birch (betula) pollen? International Journal of Biometeorology, 52, 453–462.

    Article  Google Scholar 

  • Skjøth, C. A., Sommer, J., Stach, A., Smith, M., & Brandt, J. (2007). The long range transport of birch (betula) pollen from Poland and Germany causes significant pre-season concentrations in Denmark. Clinical and Experimental Allergy, 37, 1204–1212.

    Article  Google Scholar 

  • Smith, M., Skjøth, C. A., Myszkowska, D., Uruska, A., Malgorzata, P., Stach, A., et al. (2008). Long-range transport of ambrosia pollen to Poland agricultural and forest meteorology. Agricultural and Forest Meteorology, 148, 1402–1411.

    Article  Google Scholar 

  • Soltis, P. S., Soltis, D. E., & Doyle, J. J. (1998). Molecular systematics of plants ii: DNA sequencing. Boston: Kluwer.

    Book  Google Scholar 

  • Stach, A., Smith, M., Skjøth, C. A., & Brandt, J. (2007). Examining ambrosia pollen episodes at poznañ (Poland) using back-trajectory analysis. International Journal of Biometeorology, 51, 275–286.

    Article  CAS  Google Scholar 

  • Staley, J. T., & Konopka, A. (1985). Measurement of in situ activates of non photosynthetic microorganisms in aquatic and terrestrial habitats. Annual Review of Microbiology, 24, 647–660.

    Google Scholar 

  • Sun, J., & Ariya, P. A. (2006). Atmospheric organic and bio-aerosols as cloud condensation nuclei (CCN): A review. Atmospheric Environment, 40, 795–820.

    Article  CAS  Google Scholar 

  • 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, 23–29.

    Article  Google Scholar 

  • Zhou, J., Swietlicki, E., Hansson, H. C., & Artaxo, P. (2002). Submicrometer aerosol particle size distribution and hygroscopic growth measured in the amazon rain forest during the wet season. Journal Of Geophysical Research, 107, 10 pp.

    Google Scholar 

  • ZoBell, C. E. (1946). Marine microbiology: A monograph on hydrobacteriology. Waltham, MA: Cronica Botanica.

    Google Scholar 

Download references

Acknowledgments

This study was funded by the European Commission (PASR 2006), project AeroBactics (grant agreement no. SEC6-PR-214400), and by the Swedish Research Council for Environment, Agricultural Science and Spatial Planning (FORMAS), grant no. 214-2008-1113. Niels Bohse Hendriksen made valuable comments to this article. We thank Lotte Frederiksen, Anne Grethe Holm-Jensen, Tina Thane, Pia Petersen, Kilian Smith, and Tina Šantl Temkiv for their technical assistance. We wish to acknowledge our late coauthor and colleague Runar Thyrhaug for his innovative idea of using vacuum cleaner technology in the field of aerobiology.

Author information

Author notes

  1. Karin Holmfeldt

    Present address: Ecology and Evolutionary Biology Department, University of Arizona, Tucson, AZ, 85721, USA

Authors and Affiliations

  1. Department of Cell and Molecular Biology, University of Gothenburg, Box 462, 405 30, Göteborg, Sweden

    Ulla Li Zweifel

  2. School of Natural Sciences, Linnaeus University, 391 82, Kalmar, Sweden

    Åke Hagström & Karin Holmfeldt

  3. Department of Biology, University of Bergen, PO Box 7803, 5020, Bergen, Norway

    Runar Thyrhaug

  4. Department of Environmental Science, Aarhus University, PO Box 358, 4000, Roskilde, Denmark

    Camilla Geels, Lise Marie Frohn, Carsten A. Skjøth & Ulrich Gosewinkel Karlson

Authors
  1. Ulla Li Zweifel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Åke Hagström
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karin Holmfeldt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Runar Thyrhaug
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Camilla Geels
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lise Marie Frohn
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Carsten A. Skjøth
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ulrich Gosewinkel Karlson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ulla Li Zweifel.

Additional information

Runar Thyrhaug: opus posthum.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 292 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10453-012-9250-6

Keywords

Search

Navigation