, Volume 33, Issue 4, pp 555–575 | Cite as

Seasonal variability in bacterial and fungal diversity and community composition of the near-surface atmosphere in coastal megacity

  • Ai-ling Xu
  • Zhi-wen Song
  • Xiu-lu Lang
  • Xiang Chen
  • Yan Xia
Original Paper


Bacteria and fungi are ubiquitous in the near-surface atmosphere where they may impact on the surrounding environment and human health, especially in coastal megacities. However, the diversity, composition, and seasonal variations of these airborne microbes remain limited. This study investigated the airborne microbes of the near-surface atmosphere in coastal megacity Qingdao over one year. It was found that the sample in summer displayed the highest bacterial and fungal diversity, while sample in winter exhibited the lowest bacterial and fungal diversity. Proteobacteria was the dominating bacteria, and Dothideomycetes was the most dominating fungi in the near-surface atmosphere, which took up 53–76 and 49–78% relative abundance, respectively. However, the bacterial diversity and community composition had significant seasonal variations. These data suggest that a complex set of environmental factors, including landscaping ratio, solar radiation temperature, and marine microorganisms, can affect the composition of airborne microbes in the near-surface atmosphere in coastal megacity. The analysis of the pathogenic microorganisms or opportunistic pathogenic microorganisms existed in the near-surface atmosphere revealed that the relative abundance of pathogenic microorganisms in autumn was the highest. The main pathogenic microorganisms or opportunistic pathogenic microorganisms were Acinetobacter baumannii (accounting for up to 9.93% relative abundance), Staphylococcus epidermidis (accounting for up to 11.26% relative abundance), Mycobacterium smegmatis (accounting for up to 3.68% relative abundance), Xanthomonas oryzae pv. oryzae (accounting for up to 5.36% relative abundance), which may be related to certain human or plant diseases in specific environments or at certain seasons. Therefore, the investigation of airborne microbial communities of near-surface atmosphere in coastal megacities is very important to both the understanding of airborne microbes and public health.


Microorganisms Diversity and community Atmosphere Coastal megacity 



This work was supported by the Natural Science Foundation of Shandong Province (2015ZRB01546),the National Natural Science Foundation of China (No. 31570541, 31170509), and science and technology plan projects for universities in Shandong province(J14LD05), basic research project of Qingdao (15-9-1-64-jch).


  1. Ashelford, K. E., Chuzhanova, N. A., Fry, J. C., Jones, A. J., & Weightman, A. J. (2006). New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Applied and Environmental Microbiology, 72, 5734–5741.CrossRefGoogle Scholar
  2. Bertolini, V., Gandolfi, I., & Ambrosini, R. (2013). Temporal variability and effect of environmental variables on airborne bacterial communities in an urban area of Northern Italy. Applied Microbiology and Biotechnology, 97(14), 6561–6570.CrossRefGoogle Scholar
  3. Bowers, R. M., Clements, N., Emerson, J. B., Wiedinmyer, C., Hannigan, M. P., & Fierer, N. (2013). Seasonal variability in bacterial and fungal diversity of the near -surface atmosphere. Environmental Science and Technology, 47(21), 12097–12106.CrossRefGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. Bowers, R. M., McCubbin, I. B., Hallar, A. G., & Fierer, N. (2012). Seasonal variability in airborne bacterial communities at a high-elevation site. Atmospheric Environment, 50, 41–49.CrossRefGoogle Scholar
  6. Bowers, R. M., Sullivan, A. P., Costello, E. K., Collett, J. L., Jr., Knight, R., & Fierer, N. (2011). Sources of bacteria in outdoor air across cities in the midwestern United States. Applied and Environmental Microbiology, 77, 6350–6356.CrossRefGoogle Scholar
  7. Camilla, F., Åke, H., Douglas, N., & Ulla, L. Z. (2010). Annual variations in the diversity, viability, and origin of airborne bacteria. Applied and Environmental Microbiology, 76(9), 3015–3025.CrossRefGoogle Scholar
  8. Chang, C. W., Chung, H., & Huang, C. F. (2001). Exposure of workers to airborne microorganisms in open-air swine houses [J]. Applied and Environmental Microbiology, 67(1), 155–161.CrossRefGoogle Scholar
  9. Chowdhury, S. K. R., Sangle, G. V., & Xie, X. (2009). Effects of extensively oxidized low-density lipoprotein on mitochondrial function and reactive oxygen species in porcine aortic endothelial cells. American Journal of Physiology-Endocrinology and Metabolism, 298, 89–98.CrossRefGoogle Scholar
  10. Dai, X., Wang, Y. N., & Wang, B. J. (2005). Planomicrobium chinense sp. nov., isolated from coastal sediment, and transfer of Planococcus psychrophilus and Planococcus alkanoclasticus to Planomicrobium as Planomicrobium psychrophilum comb. nov. and Planomicrobium alkanoclasticum comb. nov. International Journal of Systematic and Evolutionary Microbiology, 55(2), 699–702.CrossRefGoogle Scholar
  11. Daly, M. J. (2009). A new perspective on radiation resistance based on Deinococcus radiodurans. Nature Reviews Microbiology, 7, 237–245.CrossRefGoogle Scholar
  12. Daly, M. J., & Minton, K. W. (1995). Interchromosomal recombination in the extremely radioresistant bacterium Deinococcus radiodurans. Journal of Bacteriology, 177, 5495–5505.CrossRefGoogle Scholar
  13. De La Tour, C. B., Boisnard, S., Norais, C., Toueille, M., & Bentchikou, E. (2011). The deinococcal DdrB protein is involved in an early step of DNA double strand break repair and in plasmid transformation through its single-strand annealing activity. DNA Repair (Amst), 10, 1223–1231.CrossRefGoogle Scholar
  14. Ellwood, S. R., Syme, R. A., & Moffat, C. S. (2012). Evolution of three Pyrenophora cereal pathogens: Recent divergence, speciation and evolution of non-coding DNA. Fungal Genetics and Biology, 49, 825–829.CrossRefGoogle Scholar
  15. Fahlgren, C., Hagström, Å., Nilsson, D., & Zweife, U. L. (2010). Annual variations in the diversity, viability, and origin of airborne bacteria. Applied and Environmental Microbiology, 9(76), 3015–3025.CrossRefGoogle Scholar
  16. Ferrari, B. C., Binnerup, S. J., & Gillings, M. (2005). Microcolony cultivation on a soil substrate membrane system selects for previously uncultured soil bacteria. Applied and Environmental Microbiology, 71, 8714–8720.CrossRefGoogle Scholar
  17. Fierer, N., Liu, 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.CrossRefGoogle Scholar
  18. Franzetti, A., Gandolfi, I., Gaspari, E., Ambrosini, R., & Bestetti, G. (2011). Seasonal variability of bacteria in fine and coarse urban air particulate matter. Applied Microbiology and Biotechnology, 90, 745–753.CrossRefGoogle Scholar
  19. Ghosal, D., Omelchenko, M. V., Gaidamakova, E. K., Matrosova, V. Y., & Vasilenko, A. (2005). How radiation kills cells: Survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress. FEMS Microbiology Reviews, 29, 361–375.Google Scholar
  20. Hrynkiewicz, K., Baum, C., & Leinweber, P. (2010). Density, metabolic activity, and identity of cultivable rhizosphere bacteria on Salix viminalis in disturbed arable and landfill soils. Journal of Plant Nutrition and Soil Science, 173, 747–756.CrossRefGoogle Scholar
  21. Jaenicke, R. (2005). Abundance of cellular material and proteins in the atmosphere. Science, 308(5718), 73.CrossRefGoogle Scholar
  22. Kuffner, M., De Maria, S., Puschenreiter, M., Fallmann, K., & Wieshammer, G. (2010). Culturable bacteria from Zn- and Cd- accumulating Salix Caprea with differential effects on plant growth and heave metal availability. Journal of Applied Microbiology, 108, 1471–1484.CrossRefGoogle Scholar
  23. Lighthart, B. (2000). Mini-review of the concentration variations found in the alfresco atmospheric bacterial populations. Aerobiologia, 16(1), 7–16.CrossRefGoogle Scholar
  24. Luo, X., Zhang, J., & Li, D. (2014). Planomicrobium soli sp. nov., isolated from soil. International Journal of Systematic and Evolutionary Microbiology, 64(8), 2700–2705.CrossRefGoogle Scholar
  25. Mew, T. W. (1987). Current status and future prospects of research on bacterial blight of rice. Annual review of Phytopathology, 25, 359–382.CrossRefGoogle Scholar
  26. Munteanu, A., Uivarosi, V., & Andries, A. (2015). Recent progress in understanding the molecular mechanisms of radioresistance in Deinococcus bacteria. Extremophiles, 19(4), 707–719.CrossRefGoogle Scholar
  27. NiÑo Liu, D. O., Ronald, P. C., & Bogdanove, A. J. (2006). Xanthomonas oryzae pathovars: Model pathogens of a model crop. Molecular Plant Pathology, 7(5), 303–324.CrossRefGoogle Scholar
  28. Pavao-Zuckerman, M. A., & Coleman, D. C. (2007). Urbanization alters the functional composition, but not taxonomic diversity, of the soil nematode community. Applied Soil Ecology, 35, 329–339.CrossRefGoogle Scholar
  29. Rémi, D., Takefumi, O., & Geneviève, C. (2015). Identification of new genes contributing to the extreme radioresistance of deinococcus radiodurans using a Tn5-based transposon mutant library. PLoS ONE. doi: 10.1371/journal.pone.0124358.Google Scholar
  30. Reyrat, J. M., & Kahn, D. (2001). Mycobacterium smegmatis: An absurd model for tuberculosis? Trends in Microbiology, 9(10), 472–473.CrossRefGoogle Scholar
  31. Rogers, K. L., Fey, P. D., & Rupp, M. E. (2009). Coagulase-negative staphylococcal infections. Infectious Disease Clinics of North America, 23, 73–98.CrossRefGoogle Scholar
  32. Schloss, P. D., Westcott, S. L., & Ryabin, T. (2009). Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537–7541.CrossRefGoogle Scholar
  33. Sesartic, A., Lohmann, U., & Storelvmo, T. (2012). Bacteria in the ECHAM5-HAM global climate model. Atmospheric Chemistry and Physics, 12(18), 8645–8661.CrossRefGoogle Scholar
  34. Shahcheraghi, F., Abbasalipour, M., Feizabadi, M., Ebrahimipour, G., & Akbari, N. (2011). Isolation and genetic characterization of metallo-β-lactamase and carbapenamase producing strains of Acinetobacter baumannii from patients at Tehran hospitals. Iranian Journal of Microbiology, 3, 68–74.Google Scholar
  35. Shelton, B. G., Kirkland, K. H., & Flanders, W. D. (2002). Profiles of airborne fungi in building and outdoor environments in the Unites Stated [J]. Applied and Environmental Microbiology, 68(4), 1743–1753.CrossRefGoogle Scholar
  36. Slade, D., Lindner, A. B., Paul, G., & Radman, M. (2009). Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans. Cell, 136, 1044–1055.CrossRefGoogle Scholar
  37. Smit, E., Leeflang, P., & Glandorf, B. (1999). Analysis of fungal diversity in the wheat rhizosphere by sequencing of cloned PCR-amplified genes encoding 18S rRNA and temperature gradient gel electrophoresis[J]. Applied and Environmental Microbiology, 65(6), 2614–2621.Google Scholar
  38. Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.CrossRefGoogle Scholar
  39. Triky-Dotan, S., Ofek, M., Austerweil, M., Steiner, B., & Minz, D. (2010). Microbial aspects of accelerated degradation of metam sodium in soil. Phytopathology, 100, 367–375.CrossRefGoogle Scholar
  40. von Eiff, C., Peters, G., & Heilmann, C. (2002). Pathogenesis of infections due to coagulase-negative staphylococci. The Lancet Infectious Diseases, 2, 677–685.CrossRefGoogle Scholar
  41. Wang, G. H., Dong, J. D., & Li, X. (2010). The bacterial diversity in surface sediment from South China sea. Acta Oceanology, 29(40), 98–105.CrossRefGoogle Scholar
  42. Weinert, N., Meincke, R., Gottwald, C., Radi, V., & Dong, X. (2010). Effects of genetically modified potatoes with increased zeaxanthin content on the abundance and diversity of rhizobacteria with in vitro antagonistic activity do not exceed natural variability among cultivars. Plant and Soil, 326, 437–452.CrossRefGoogle Scholar
  43. Yamaguchi, N., Park, J., & Kodama, M. (2014). Changes in the airborne bacterial community in outdoor environments following Asian dust events. Microbes and Environments, 29(1), 82–88.CrossRefGoogle Scholar
  44. Yoon, J. H., Kang, S. S., & Lee, K. C. (2001). Planomicrobium koreense gen. nov., sp. nov., a bacterium isolated from the Korean traditional fermented seafood jeotgal, and transfer of Planococcus okeanokoites (Nakagawa et al. 1996) and Planococcus mcmeekinii (Junge et al. 1998) to the genus Planomicrobium. International Journal of Systematic and Evolutionary Microbiology, 51(4), 1511–1520.CrossRefGoogle Scholar
  45. Zahradka, K., Slade, D., Bailone, A., Sommer, S., & Averbeck, D. (2006). Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature, 443, 569–573.Google Scholar
  46. Zhang, D. C., Liu, H. C., & Xin, Y. H. (2009). Planomicrobium glaciei sp. nov., a psychrotolerant bacterium isolated from a glacier. International Journal of Systematic and Evolutionary Microbiology, 59(6), 1387–1390.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Ai-ling Xu
    • 1
  • Zhi-wen Song
    • 1
  • Xiu-lu Lang
    • 1
  • Xiang Chen
    • 1
  • Yan Xia
    • 1
  1. 1.School of Environmental and Municipal EngineeringQingdao Technological UniversityQingdaoChina

Personalised recommendations