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Seasonal variations in airborne bacterial community structures at a suburban site of central Japan over a 1-year time period using PCR-DGGE method

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Abstract

Airborne bacteria could affect human health and climate. In this study, the bacterial community structures were investigated by analyzing air samples collected from a suburban location in Toyama, central Japan. Sixty samples were collected almost weekly between March 2009 and February 2010. A cultivation-independent approach, PCR plus denaturing gradient gel electrophoresis (DGGE), was used to analyze changes in the structure of the airborne bacterial communities. The DGGE profiles showed significant differences between sampling days, reflecting quite different bacterial profiles. Sequencing of DGGE bands revealed that the bacterial community was dominated by γ-Proteobacteria, Firmicutes, α-Proteobacteria, Bacteroidetes, and Actinobacteria. The most frequently observed genus was Pseudomonas, followed by Bacillus. The airborne bacterial assemblage in winter differed from that in the other seasons. The differences could be attributed a number of factors, such as temperature, relative humidity, wind direction, and snowfall. In spring, the largest number of bands was classified as plant chloroplasts, such as Japanese cedar (Cryptomeria japonica) and Pinus spp., which are the major pollen allergen sources in Japan. The airborne bacterial abundance estimated by real-time TaqMan PCR ranged from 1.1 × 103 to 1.3 × 105 cells m−3.

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References

  • Bertolini, V., Gandolfi, I., Ambrosini, R., Bestetti, G., Innocente, E., Rampazzo, G., et al. (2013). Temporal variability and effect of environmental variables on airborne bacterial communities in an urban area of Northern Italy. Applied Microbiology and Biotechnology, 97, 6561–6570.

    Article  CAS  Google Scholar 

  • Blanchard, D. C., & Syzdek, L. D. (1982). Water-to-air transfer and enrichment of bacteria in drops from bursting bubbles. Applied and Environmental Microbiology, 43, 1001–1005.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Bowers, R. M., McLetchie, S., Knight, R., & Fierer, N. (2011). Spatial variability in airborne bacterial communities across land-use types and their relationship to the bacterial communities of potential source environments. The ISME Journal, 5, 601–612.

    Article  CAS  Google Scholar 

  • 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 of the United States of America, 104, 299–304.

    Article  CAS  Google Scholar 

  • 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, 9, 9263–9280.

    Article  CAS  Google Scholar 

  • Christner, B. C., Cai, R., Morris, C. E., McCarter, K. S., Foreman, C. M., Skidmore, M. L., et al. (2008). 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 of the United States of America, 105, 18854–18859.

    Article  CAS  Google Scholar 

  • Claesson, M. J., Wang, Q., O’Sullivan, O., Greene-Diniz, R., Cole, J. R., Ross, R. P., et al. (2010). Comparison of two next-generation sequencing technologies for resolving highly complex microbiota composition using tandem variable 16S rRNA gene regions. Nucleic Acids Research, 38, e200.

    Article  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, A., 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 

  • Fannin, K. F., Vana, S. C., & Jakubowski, W. (1985). Effect of an activated sludge wastewater treatment plant on ambient air densities of aerosols containing bacteria and viruses. Applied and Environmental Microbiology, 49, 1191–1196.

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Gao, B., Mohan, R., & Gupta, R. S. (2009). Phylogenomics and protein signatures elucidating the evolutionary relationships among the Gammaproteobacteria. International Journal of Systematic and Evolutionary Microbiology, 59, 234–247.

    Article  CAS  Google Scholar 

  • Griffin, D. W., Garrison, V. H., Herman, J. R., & Shinn, E. A. (2001). African desert dust in the Caribbean atmosphere: Microbiology and public health. Aerobiologia, 17, 203–213.

    Article  Google Scholar 

  • Gupta, R. S., & Lorenzini, E. (2007). Phylogeny and molecular signatures (conserved proteins and indels) that are specific for the Bacteroidetes and Chlorobi species. BMC Evolutionary Biology, 7, 71.

    Article  Google Scholar 

  • Gupta, R. S., & Mok, A. (2007). Phylogenomics and signature proteins for the alpha proteobacteria and its main groups. BMC Microbiology, 7, 106.

    Article  Google Scholar 

  • Haakensen, M., Dobson, C. M., Deneer, H., & Ziola, B. (2008). Real-time PCR detection of bacteria belonging to the Firmicutes Phylum. International Journal of Food Microbiology, 125, 236–241.

    Article  CAS  Google Scholar 

  • Hanning, I. B., & Ricke, S. C. (2011). Prescreening of microbial populations for the assessment of sequencing potential. Methods in Molecular Biology, 733, 159–170.

    Article  CAS  Google Scholar 

  • Harms, G., Layton, A. C., Dionisi, H. M., Gregory, I. R., Garrett, V. M., Hawkins, S. A., et al. (2003). Real-time PCR quantification of nitrifying bacteria in a municipal wastewater treatment plant. Environmental Science and Technology, 37, 343–351.

    Article  CAS  Google Scholar 

  • Harrison, R. M., Jones, A. M., Biggins, P. D. E., Pomeroy, N., Cox, C. S., Kidd, S. P., et al. (2005). Climate factors influencing bacterial count in background air samples. International Journal of Biometeorology, 49, 167–178.

    Article  Google Scholar 

  • Jaenicke, R. (2005). Abundance of cellular material and proteins in the atmosphere. Science, 308, 73.

    Article  CAS  Google Scholar 

  • Jeon, E. M., Kim, H. J., Jung, K., Kim, J. H., Kim, M. Y., Kim, Y. P., et al. (2011). Impact of Asian dust events on airborne bacterial community assessed by molecular analyses. Atmospheric Environment, 45, 4313–4321.

    Article  CAS  Google Scholar 

  • Jones, A. M., & Harrison, R. M. (2004). The effects of meteorological factors on atmospheric bioaerosol concentrations—A review. Science of the Total Environment, 326, 151–180.

    Article  CAS  Google Scholar 

  • Klappenbach, J. A., Saxman, P. R., Cole, J. R., & Schmidt, T. M. (2001). rrndb: The ribosomal RNA operon copy number database. Nucleic Acids Research, 29, 181–184.

    Article  CAS  Google Scholar 

  • Kuske, C. R. (2006). Current and emerging technologies for the study of bacteria in the outdoor air. Current Opinion in Biotechnology, 17, 291–296.

    Article  CAS  Google Scholar 

  • Lee, S., Choi, B., Yi, S. M., & Ko, G. (2009). Characterization of microbial community during Asian dust events in Korea. Science of the Total Environment, 407, 5308–5314.

    Article  CAS  Google Scholar 

  • Lee, S. H., Lee, H. J., Kim, S. J., Lee, H. M., Kang, H., & Kim, Y. P. (2010). Identification of airborne bacterial and fungal community structures in an urban area by T-RFLP analysis and quantitative real-time PCR. Science of the Total Environment, 408, 1349–1357.

    Article  CAS  Google Scholar 

  • Li, K. (2011). Molecular comparison of the sampling efficiency of four types of airborne bacterial samplers. Science of the Total Environment, 409, 5493–5498.

    Article  CAS  Google Scholar 

  • Li, K., Dong, S., Wu, Y., & Yao, M. (2010). Comparison of the biological content of air samples collected at ground level and at higher elevation. Aerobiologia, 26, 233–244.

    Article  Google Scholar 

  • Maki, T., Susuki, S., Kobayashi, F., Kakikawa, M., Tobo, Y., Yamada, M., et al. (2010). Phylogenetic analysis of atmospheric halotolerant bacterial communities at high altitude in an Asian dust (KOSA) arrival region, Suzu City. Science of the Total Environment, 408, 4556–4562.

    Article  CAS  Google Scholar 

  • Marcos, C., Rodriguez, F. J., Luna, I., Jato, V., & González, R. (2001). Pinus pollen aerobiology and clinical sensitization in northwest Spain. Annals of Allergy, Asthma & Immunology, 87, 39–42.

    Article  CAS  Google Scholar 

  • Maron, P. A., Mougel, C., Lejon, D. P. H., Carvalho, E., Bizet, K., Marck, G., et al. (2006). Temporal variability of airborne bacterial community structure in an urban area. Atmospheric Environment, 40, 8074–8080.

    Article  CAS  Google Scholar 

  • Matthias-Maser, S., Obolkin, V., Khodzer, T., & Jaenicke, R. (2000). Seasonal variation of primary biological aerosol particles in the remote continental region of Lake Baikal/Siberia. Atmospheric Environment, 34, 3805–3811.

    Article  CAS  Google Scholar 

  • Muyzer, G., de Waal, E. C., & Uitterlinden, A. G. (1993). Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology, 59, 695–700.

    CAS  Google Scholar 

  • Muyzer, G., & Smalla, K. (1998). Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie van Leeuwenhoek, 73, 127–141.

    Article  CAS  Google Scholar 

  • Muyzer, G., Teske, A., Wirsen, C. O., & Jannasch, H. W. (1995). Phylogenetic relationships of Thiomicrospira species and their identification in deep-sea hydrothermal vent samples by denaturing gradient gel electrophoresis of 16S rDNA fragments. Archives of Microbiology, 164, 165–172.

    Article  CAS  Google Scholar 

  • Neale, D. B., & Sederoff, R. R. (1989). Paternal inheritance of chloroplast DNA and maternal inheritance of mitochondrial DNA in loblolly pine. Theoretical and Applied Genetics, 77, 212–216.

    Article  CAS  Google Scholar 

  • Negrin, M. M., Del Panno, M. T., & Ronco, A. E. (2007). Study of bioaerosols and site influence in the La Plata area (Argentina) using conventional and DNA (fingerprint) based methods. Aerobiologia, 23, 249–258.

    Article  Google Scholar 

  • Nehme, B., Létourneau, V., Forster, R. J., Veillette, M., & Duchaine, C. (2008). Culture-independent approach of the bacterial bioaerosol diversity in the standard swine confinement buildings, and assessment of the seasonal effect. Environmental Microbiology, 10, 665–675.

    Article  CAS  Google Scholar 

  • Nicholson, W. L., Munakata, N., Horneck, G., Melosh, H. J., & Setlow, P. (2000). Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiology and Molecular Biology Reviews, 64, 548–572.

    Article  CAS  Google Scholar 

  • Nishimura, Y., Kenzaka, T., Sueyoshi, A., Li, P., Fujiyama, H., Baba, T., et al. (2010). Similarity of bacterial community structure between Asian dust and its sources determined by rRNA gene-targeted approaches. Microbes and Environments, 25, 22–27.

    Article  Google Scholar 

  • Ohba, K., Iwakawa, M., Okada, Y., & Murai, M. (1971). Paternal transmission of a plastid anomaly in some reciprocal crosses of Sugi Cryptomeria japonica D. Don. Silvae Genetica, 20, 101–107.

    Google Scholar 

  • Okubo, K., Ogino, S., Nagakura, T., & Ishikawa, T. (2006). Omalizumab is effective and safe in the treatment of Japanese cedar pollen-induced seasonal allergic rhinitis. Allergology International, 55, 379–386.

    Article  CAS  Google Scholar 

  • Peccia, J., & Hernandez, M. (2006). Incorporating polymerase chain reaction-based identification, population characterization, and quantification of microorganisms into aerosol science: a review. Atmospheric Environment, 40, 3941–3961.

    Article  CAS  Google Scholar 

  • Ranjard, L., Poly, F., & Nazaret, S. (2000). Monitoring complex bacterial communities using culture-independent molecular techniques: application to soil environment. Research in Microbiology, 151, 167–177.

    Article  CAS  Google Scholar 

  • Raven, J. A., & Allen, J. F. (2003). Genomics and chloroplast evolution: What did cyanobacteria do for plants? Genome Biology, 4, 209.

    Article  Google Scholar 

  • Servin, J. A., Herbold, C. W., Skophammer, R. G., & Lake, J. A. (2008). Evidence excluding the root of the tree of life from the actinobacteria. Molecular Biology and Evolution, 25, 1–4.

    Article  CAS  Google Scholar 

  • Shaffer, B. T., & Lighthart, B. (1997). Survey of culturable airborne bacteria at four diverse locations in Oregon: Urban, rural, forest, and coastal. Microbial Ecology, 34, 167–177.

    Article  Google Scholar 

  • Shen, F., & Yao, M. (2013). Are we biologically safe with snow precipitation? A case study in Beijing. PLoS ONE, 8, e65249.

    Article  CAS  Google Scholar 

  • Tanaka, D., Tokuyama, Y., Terada, Y., Kunimochi, K., Mizumaki, C., Tamura, S., et al. (2011). Bacterial communities in Asian dust-containing snow layers on Mt. Tateyama, Japan. Bulletin of Glaciological Research, 29, 31–39.

    Article  Google Scholar 

  • Ventura, M., Canchaya, C., Tauch, A., Chandra, G., Fitzgerald, G. F., Chater, K. F., et al. (2007). Genomics of Actinobacteria: Tracing the evolutionary history of an ancient phylum. Microbiology and Molecular Biology Reviews, 71, 495–548.

    Article  CAS  Google Scholar 

  • Ward, D. M., Weller, R., & Bateson, M. M. (1990). 16S rRNA sequences reveal numerous uncultured microorganisms in a natural community. Nature, 345, 63–65.

    Article  CAS  Google Scholar 

  • Xu, Z., & Yao, M. (2013). Monitoring of bioaerosol inhalation risks in different environments using a six-stage Andersen sampler and the PCR-DGGE method. Environmental Monitoring and Assessment, 185, 3993–4003.

    Article  CAS  Google Scholar 

  • 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, 481–498.

    Article  Google Scholar 

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Acknowledgments

This work was supported by the Japan Society for the Promotion of Science KAKENHI Grant Numbers 22510026 and 25340055.

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Correspondence to Daisuke Tanaka.

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Tanaka, D., Terada, Y., Nakashima, T. et al. Seasonal variations in airborne bacterial community structures at a suburban site of central Japan over a 1-year time period using PCR-DGGE method. Aerobiologia 31, 143–157 (2015). https://doi.org/10.1007/s10453-014-9353-3

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  • DOI: https://doi.org/10.1007/s10453-014-9353-3

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