Abstract
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.
Similar content being viewed by others
References
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Daly, M. J. (2009). A new perspective on radiation resistance based on Deinococcus radiodurans. Nature Reviews Microbiology, 7, 237–245.
Daly, M. J., & Minton, K. W. (1995). Interchromosomal recombination in the extremely radioresistant bacterium Deinococcus radiodurans. Journal of Bacteriology, 177, 5495–5505.
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.
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.
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.
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.
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.
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.
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.
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.
Jaenicke, R. (2005). Abundance of cellular material and proteins in the atmosphere. Science, 308(5718), 73.
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.
Lighthart, B. (2000). Mini-review of the concentration variations found in the alfresco atmospheric bacterial populations. Aerobiologia, 16(1), 7–16.
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.
Mew, T. W. (1987). Current status and future prospects of research on bacterial blight of rice. Annual review of Phytopathology, 25, 359–382.
Munteanu, A., Uivarosi, V., & Andries, A. (2015). Recent progress in understanding the molecular mechanisms of radioresistance in Deinococcus bacteria. Extremophiles, 19(4), 707–719.
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.
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.
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.
Reyrat, J. M., & Kahn, D. (2001). Mycobacterium smegmatis: An absurd model for tuberculosis? Trends in Microbiology, 9(10), 472–473.
Rogers, K. L., Fey, P. D., & Rupp, M. E. (2009). Coagulase-negative staphylococcal infections. Infectious Disease Clinics of North America, 23, 73–98.
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.
Sesartic, A., Lohmann, U., & Storelvmo, T. (2012). Bacteria in the ECHAM5-HAM global climate model. Atmospheric Chemistry and Physics, 12(18), 8645–8661.
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.
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.
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.
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.
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.
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.
von Eiff, C., Peters, G., & Heilmann, C. (2002). Pathogenesis of infections due to coagulase-negative staphylococci. The Lancet Infectious Diseases, 2, 677–685.
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.
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.
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.
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.
Zahradka, K., Slade, D., Bailone, A., Sommer, S., & Averbeck, D. (2006). Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature, 443, 569–573.
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.
Acknowledgements
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).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Xu, Al., Song, Zw., Lang, Xl. et al. Seasonal variability in bacterial and fungal diversity and community composition of the near-surface atmosphere in coastal megacity. Aerobiologia 33, 555–575 (2017). https://doi.org/10.1007/s10453-017-9489-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10453-017-9489-z