Skip to main content
Log in

Microbial characteristics of culturable fungi and bacteria in aerosol particles of a coastal region

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

Abstract

In this study, atmospheric bioaerosol particles were collected from March to December 2015 in the coastal region of Qingdao. The dominant fungi were identified, and the concentrations and size distributions of bacteria, total fungi and dominant fungi were measured. The most dominant fungal taxon was Cladosporium, followed by Alternaria, Penicillium and Aspergillus. The concentrations of fungi showed significant seasonal variation (p < 0.05) and peaked in summer, while bacterial concentrations peaked in autumn without significant seasonal differences. The particle size of fungi showed a similar normal distribution, peaking at 2.1 to 3.3 μm, while that of bacteria presented a skewed distribution pattern with a peak at > 7.0 μm. The size patterns of the four dominant fungi were distinct due to their respective properties. With correlation analysis, we found PM10, CO and NO2 were positively associated with the bacterial concentration. The factors correlated with fungal concentrations included temperature, relative humidity, CO, NO2, SO2 and O3. The results of RDA showed that the most important meteorological factors affecting the microorganism species composition were temperature and relative humidity, and the dominant air pollutants were SO2, CO and O3. We selected related parameters to conduct multiple linear regression analysis to explore the synergistic effects on a given microorganism. The contribution to the rate of changes in bacterial and fungal concentrations caused by related factors was less than 30%, indicating that the sources and community changes had a great influence on bioaerosol concentrations. The more detailed the classification of microorganisms is, the more specific correlation information may be obtained through our analysis method.

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

Access this article

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Ariya, P. A., & Amyot, M. (2004). New directions: The role of bioaerosols in atmospheric chemistry and physics. Atmospheric Environment, 38(8), 1231–1232.

    CAS  Google Scholar 

  • Adhikari, A., Reponen, T., Grinshpun, S. A., Martuzevicius, D., & LeMasters, G. (2006). Correlation of ambient inhalable bioaerosols with particulate matter and ozone: A two-year study. Environmental Pollution, 140(1), 16–28.

    CAS  Google Scholar 

  • Awad, A. H. A. (2005). Vegetation: A source of air fungal bio-contaminant. Aerobiologia, 21(1), 53–61.

    Google Scholar 

  • Aydogdu, H., Asan, A., & Otkun, M. T. (2010). Indoor and outdoor airborne bacteria in child day-care centers in Edirne City (Turkey), seasonal distribution and influence of meteorological factors. Environmental Monitoring and Assessment, 164(1–4), 53–66.

    CAS  Google Scholar 

  • Bovallius, A. K. E., Bucht, B., Roffey, R., & Anäs, P. (1978). Three-year investigation of the natural airborne bacterial flora at four localities in Sweden. Applied and Environmental Microbiology, 35(5), 847–852.

    CAS  Google Scholar 

  • Bauer, H., Giebl, H., Hitzenberger, R., Kasper-Giebl, A., Reischl, G., Zibuschka, F., et al. (2003). Airborne bacteria as cloud condensation nuclei. Journal of Geophysical Research: Atmospheres, 108(D21), 4658.

    Google Scholar 

  • Bartlett, K. H., Kennedy, S. M., Brauer, M., Van Netten, C., & Dill, B. (2004). Evaluation and a predictive model of airborne fungal concentrations in school classrooms. Annals of Occupational Hygiene, 48(6), 547–554.

    Google Scholar 

  • 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 & Technology, 47(21), 12097–12106.

    CAS  Google Scholar 

  • Brągoszewska, E., Mainka, A., & Pastuszka, J. (2017). Concentration and size distribution of culturable bacteria in ambient air during spring and winter in Gliwice: a typical urban area. Atmosphere, 8(12), 239.

    Google Scholar 

  • Burch, M., & Levetin, E. (2002). Effects of meteorological conditions on spore plumes. International Journal of Biometeorology, 46(3), 107–117.

    CAS  Google Scholar 

  • Burge, H. A., & Rogers, C. A. (2000). Outdoor allergens. Environmental Health Perspectives, 108, 653–659.

    CAS  Google Scholar 

  • Cooley, J. D., Wong, W. C., Jumper, C. A., & Straus, D. C. (1998). Correlation between the prevalence of certain fungi and sick building syndrome. Occupational and Environmental Medicine, 55(9), 579–584.

    CAS  Google Scholar 

  • Chen, X., Ran, P., Ho, K., Lu, W., Li, B., Gu, Z., et al. (2012). Concentrations and size distributions of airborne microorganisms in Guangzhou during summer. Aerosol and Air Quality Research, 12(6), 1336–1344.

    Google Scholar 

  • Celenk, S., Bicakci, A., Erkan, P., & Aybeke, M. (2007). Cladosporium Link ex Fr. and Alternaria Nees ex Fr. spores in the atmosphere of Edirne. International Journal Biological Environment Sciences, 1, 127–130.

    Google Scholar 

  • Cao, C., Jiang, W., Wang, B., Fang, J., Lang, J., Tian, G., et al. (2014). Inhalable microorganisms in Beijing’s PM2.5 and PM10 pollutants during a severe smog event. Environmental Science & Technology, 48(3), 1499–1507.

    CAS  Google Scholar 

  • Delort, A. M., Vaïtilingom, M., Amato, P., Sancelme, M., Parazols, M., Mailhot, G., et al. (2010). A short overview of the microbial population in clouds: Potential roles in atmospheric chemistry and nucleation processes. Atmospheric Research, 98(2–4), 249–260.

    CAS  Google Scholar 

  • Dong, L., Qi, J., Shao, C., Zhong, X., Gao, D., Cao, W., et al. (2016). Concentration and size distribution of total airborne microbes in hazy and foggy weather. Science of the Total Environment, 541, 1011–1018.

    CAS  Google Scholar 

  • Fang, Z., Ouyang, Z., Hu, L., Lin, X., & Wang, X. (2004). Granularity distribution of airborne microbes in summer in Beijing. Environmental Science, 25(6), 1–5. (in Chinese).

    Google Scholar 

  • Fang, Z., Ouyang, Z., Hu, L., Wang, X., Zheng, H., & Lin, X. (2005). Culturable airborne fungi in outdoor environments in Beijing, China. Science of the Total Environment, 350, 47–58.

    CAS  Google Scholar 

  • Fang, Z., Ouyang, Z., Zheng, H., & Wang, X. (2008). Concentration and size distribution of culturable airborne microorganisms in outdoor environments in Beijing, China. Aerosol Science and Technology, 42(5), 325–334.

    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.

    Google Scholar 

  • Gupta, S. K., Pereira, B. M. J., & Singh, A. B. (1993). Survey of airborne culturable and non-culturable fungi at different sites in Delhi metropolis. Asian Pacific Journal of Allergy and Immunology, 11(1), 19.

    CAS  Google Scholar 

  • Giner, M. M., & García, J. C. (1995). Daily variations of Alternaria spores in the city of Murcia (semi-arid southeastern Spain). International Journal of Biometeorology, 38(4), 176–179.

    Google Scholar 

  • Gottwald, T. R., Trocine, T. M., & Timmer, L. W. (1997). A computer-controlled environmental chamber for the study of aerial fungal spore release. Phytopathology, 87(10), 1078–1084.

    CAS  Google Scholar 

  • Grinn-Gofroń, A., & Rapiejko, P. (2009). Occurrence of Cladosporium spp. and Alternaria spp. spores in Western, Northern and Central-Eastern Poland in 2004–2006 and relation to some meteorological factors. Atmospheric Research, 93(4), 747–758.

    Google Scholar 

  • Gautam, S., Kumar, P., & Patra, A. K. (2016). Occupational exposure to particulate matter in three Indian opencast mines. Air Quality, Atmosphere & Health, 9(2), 143–158.

    CAS  Google Scholar 

  • Hargreaves, M., Parappukkaran, S., Morawska, L., Hitchins, J., He, C., & Gilbert, D. (2003). A pilot investigation into associations between indoor airborne fungal and non-biological particle concentrations in residential houses in Brisbane, Australia. Science of the Total Environment, 312(1–3), 89–101.

    CAS  Google Scholar 

  • Hu, L., Fang, Z., Ouyang, Z., Liao, X., Lin, X., & Wang, X. (2005). Ecological distributions of airborne fungi in outdoor environments in Beijing, China. Environmental Science, 26(5), 22–27. (in Chinese).

    CAS  Google Scholar 

  • Hameed, A. A., Khoder, M. I., Yuosra, S., Osman, A. M., & Ghanem, S. (2009). Diurnal distribution of airborne bacteria and fungi in the atmosphere of Helwan area, Egypt. Science of the Total Environment, 407(24), 6217–6222.

    Google Scholar 

  • Harrison, R. M., Jones, A. M., Biggins, P. D., 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(3), 167–178.

    Google Scholar 

  • Ho, H. M., Rao, C. Y., Hsu, H. H., Chiu, Y. H., Liu, C. M., & Chao, H. J. (2005). Characteristics and determinants of ambient fungal spores in Hualien, Taiwan. Atmospheric Environment, 39(32), 5839–5850.

    CAS  Google Scholar 

  • Hameed, A. A., Khoder, M. I., Ibrahim, Y. H., Saeed, Y., Osman, M. E., & Ghanem, S. (2012). Study on some factors affecting survivability of airborne fungi. Science of the Total Environment, 414, 696–700.

    Google Scholar 

  • Haas, D., Galler, H., Luxner, J., Zarfel, G., Buzina, W., Friedl, H., et al. (2013). The concentrations of culturable microorganisms in relation to particulate matter in urban air. Atmospheric Environment, 65, 215–222.

    CAS  Google Scholar 

  • Hu, Q., & Cai, Z. (1994). Research on atmospheric mivroorganisms in Shenyang city. Environmental Protection Science, 21(6), 353–356. (in Chinese).

    Google Scholar 

  • Humbal, C., Joshi, S. K., Trivedi, U. K., & Gautam, S. (2019). Evaluating the colonization and distribution of fungal and bacterial bio-aerosol in Rajkot, western India using multi-proxy approach. Air Quality, Atmosphere & Health, 12(6), 693–704.

    CAS  Google Scholar 

  • Hwang, S. H., Park, W. M., Ahn, J. K., Lee, K. J., Min, K. B., & Park, J. B. (2016). Relationship between culturable airborne bacteria concentrations and ventilation systems in underground subway stations in Seoul, South Korea. Air Quality, Atmosphere & Health, 9(2), 173–178.

    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(1–3), 151–180.

    CAS  Google Scholar 

  • Jones, R., Recer, G. M., Hwang, S. A., & Lin, S. (2011). Association between indoor mold and asthma among children in Buffalo, New York. Indoor Air, 21(2), 156–164.

    CAS  Google Scholar 

  • Jin, C., 2011. Community of airborne microbes in bioserosol in the Qingdao coastal region. Master thesis. Ocean University of China, Qingdao (in Chinese).

  • Katial, R. K., Zhang, Y., Jones, R. H., & Dyer, P. D. (1997). Atmospheric mold spore counts in relation to meteorological parameters. International Journal of Biometeorology, 41(1), 17–22.

    CAS  Google Scholar 

  • Lighthart, B. (1973). Survival of airborne bacteria in a high urban concentration of carbon monoxide. Applied Environmental Microbiology, 25(1), 86–91.

    CAS  Google Scholar 

  • Lyon, F. L., Kramer, C. L., & Eversmeyer, M. G. (1984). Variation of airspora in the atmosphere due to weather conditions. Grana, 23(3), 177–181.

    Google Scholar 

  • Lighthart, B., Shaffer, B. T., Marthi, B., & Ganio, L. (1991). Trajectory of aerosol droplets from a sprayed bacterial suspension. Applied Environmental Microbiology, 57(4), 1006–1012.

    CAS  Google Scholar 

  • Lighthart, B., & Shaffer, B. T. (1994). Bacterial flux from chaparral into the atmosphere in mid-summer at a high desert location. Atmospheric Environment, 28(7), 1267–1274.

    Google Scholar 

  • Levetin, E., Shaughnessy, R., Fisher, E., Ligman, B., Harrison, J., & Brennan, T. (1995). Indoor air quality in schools: Exposure to fungal allergens. Aerobiologia, 11(1), 27–34.

    Google Scholar 

  • Li, D. W., & Kendrick, B. (1995). A year-round study on functional relationships of airborne fungi with meteorological factors. International Journal of Biometeorology, 39(2), 74–80.

    CAS  Google Scholar 

  • Lee, N., Hui, D., Wu, A., Chan, P., Cameron, P., Joynt, G. M., et al. (2003). A major outbreak of severe acute respiratory syndrome in Hong Kong. New England Journal of Medicine, 348(20), 1986–1994.

    Google Scholar 

  • Lin, W., & Li, C. (2000). Associations of fungal aerosols, air pollutants, and meteorological factors. Aerosol Science & Technology, 32(4), 359–368.

    CAS  Google Scholar 

  • Lee, S., Ghim, Y. S., Kim, S. W., & Yoon, S. C. (2010). Effect of biomass burning and regional background aerosols on CCN activity derived from airborne in-situ measurements. Atmospheric Environment, 44(39), 5227–5236.

    CAS  Google Scholar 

  • Lighthart, B., & Shaffer, B. T. (1995). Viable bacteria aerosol particle size distributions in the midsummer atmosphere at an isolated location in the high desert chaparral. Aerobiologia, 11(1), 19–25.

    Google Scholar 

  • Li, Y., Fu, H., Wang, W., Liu, J., Meng, Q., & Wang, W. (2015). Characteristics of bacterial and fungal aerosols during the autumn haze days in Xi'an, China. Atmospheric Environment, 122, 439–447.

    CAS  Google Scholar 

  • Li, Y., Lu, R., Li, W., Xie, Z., & Song, Y. (2017). Concentrations and size distributions of viable bioaerosols under various weather conditions in a typical semi-arid city of Northwest China. Journal of Aerosol Science, 106, 83–92.

    CAS  Google Scholar 

  • Liu, M. M. (2008). Study on distribution of bioaerosol in fall and winter in Qingdao coastal region. Master thesis. Ocean University of China, Qingdao. (in Chinese).

  • Macher, J. M. (1989). Positive-hole correction of multiple-jet impactors for collecting viable microorganisms. American Industrial Hygiene Association Journal, 50(11), 561–568.

    CAS  Google Scholar 

  • Maier, R. M., Pepper, I. L., & Gerba, C. P. (2010). Environmental microbiology, seconded (p. 125). Beijing, China: Science press.

    Google Scholar 

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

    CAS  Google Scholar 

  • Medrela-Kuder, E. (2003). Seasonal variations in the occurrence of culturable airborne fungi in outdoor and indoor air in Cracow. International Biodeterioration & Biodegradation, 52(4), 203–205.

    Google Scholar 

  • Montero, A., Dueker, M. E., & O’Mullan, G. D. (2016). Culturable bioaerosols along an urban waterfront are primarily associated with coarse particles. PeerJ, 4, e2827.

    Google Scholar 

  • Mouli, P., Mohan, S., & Reddy, S. (2005). Assessment of microbial(bacteria) concentrations of ambient air at semi-arid urban region: Influence of meteorological factors. Applied Ecology and Environmental Research, 3(2), 139–149.

    Google Scholar 

  • O’Connor, D. J., Sadyś, M., Skjøth, C. A., Healy, D. A., Kennedy, R., & Sodeau, J. R. (2014). Atmospheric concentrations of Alternaria, Cladosporium, Ganoderma and Didymella spores monitored in Cork (Ireland) and Worcester (England) during the summer of 2010. Aerobiologia, 30(4), 397–411.

    Google Scholar 

  • Pasanen, A. L., Pasanen, P., Jantunen, M. J., & Kalliokoski, P. (1991). Significance of air humidity and air velocity for fungal spore release into the air. Atmospheric Environment. Part A. General Topics, 25(2), 459–462.

    Google Scholar 

  • Polymenakou, P. N. (2012). Atmosphere: a source of pathogenic or beneficial microbes? Atmosphere, 3(1), 87–102.

    Google Scholar 

  • Reponen, T., Grinshpun, S. A., Conwell, K. L., Wiest, J., & Anderson, M. (2001). Aerodynamic versus physical size of spores: measurement and implication for respiratory deposition. Grana, 40(3), 119–125.

    Google Scholar 

  • Raisi, L., Aleksandropoulou, V., Lazaridis, M., & Katsivela, E. (2013). Size distribution of viable, cultivable, airborne microbes and their relationship to particulate matter concentrations and meteorological conditions in a Mediterranean site. Aerobiologia, 29, 233–248.

    Google Scholar 

  • Salvaggio, J., & Aukrust, L. (1981). Mold-induced asthma. Journal of Allergy & Clinical Immunology, 68(5), 327–346.

    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(3), 167–177.

    CAS  Google Scholar 

  • Song, L., Song, W., & Wei, S. (1999). Study on airborne bacteria pollution in Shanghai. Shanghai Environment Science, 18, 258–260. (in Chinese).

    Google Scholar 

  • Shelton, B. G., Kirkland, K. H., Flanders, W. D., & Morris, G. K. (2002). Profiles of airborne fungi in buildings and outdoor environments in the United States. Applied and Environmental Microbiology, 68(4), 1743–1753.

    CAS  Google Scholar 

  • Salonen, H., Duchaine, C., Mazaheri, M., Clifford, S., & Morawska, L. (2015a). Airborne culturable fungi in naturally ventilated primary school environments in a subtropical climate. Atmospheric Environment, 106, 412–418.

    CAS  Google Scholar 

  • Salonen, H., Duchaine, C., Mazaheri, M., Clifford, S., Lappalainen, S., Reijula, K., et al. (2015b). Airborne viable fungi in school environments in different climatic regions–A review. Atmospheric Environment, 104, 186–194.

    CAS  Google Scholar 

  • Sidel, F. F. B., Bouziane, H., del Mar Trigo, M., El Haskouri, F., Bardei, F., Redouane, A., et al. (2015). Airborne fungal spores of Alternaria, meteorological parameters and predicting variables. International Journal of Biometeorology, 59(3), 339–346.

    Google Scholar 

  • Singh, A. B., Chatterji, M., Singh, B. P., & Gangal, S. V. (1990). Airborne viable fungi in library: Before and after agitation of books. Indian Journal of Aerobiology, 3, 32–38.

    Google Scholar 

  • Tong, Y., & Lighthart, B. (2000). The annual bacterial particle concentration and size distribution in the ambient atmosphere in a rural area of the Willamette Valley, Oregon. Aerosol Science & Technology, 32(5), 393–403.

    CAS  Google Scholar 

  • Tian, Y., Ju, T. Z., Feng, K., Ma, Y., Suo, A., & Zhang, J. (2008). Analysis of air bacterium pollution in function area and sterilization effect of urban greenbelt system in Lanzhou city. Environmental Monitoring in China, 19, 45–47.

    CAS  Google Scholar 

  • Theunissen, H. J., Lemmens-den Toom, N. A., Burggraaf, A., Stolz, E., & Michel, M. F. (1993). Influence of temperature and relative humidity on the survival of Chlamydia pneumoniae in aerosols. Applied and Environmental Microbiology, 59(8), 2589–2593.

    CAS  Google Scholar 

  • Vermani, M., Vijayan, V. K., Kausar, M. A., & Agarwal, M. K. (2010). Quantification of airborne Aspergillus allergens: redefining the approach. Journal of Asthma, 47(7), 754–761.

    Google Scholar 

  • Wu, Y., Chan, C., Rao, C. Y., Lee, C., Hsu, H., Chiu, Y., et al. (2007). Characteristics, determinants, and spatial variations of ambient fungal levels in the subtropical Taipei metropolis. Atmospheric Environment, 41(12), 2500–2509.

    CAS  Google Scholar 

  • Wang, C., Xie, X., Zeng, H., Ouyang, Y., Zheng, Z., & Chen, Y. (2008). Monitoring analysis of air microbial pollution conditions in Shenzhen city. Journal of Microbiology, 28, 93–97. (in Chinese).

    Google Scholar 

  • Wu, Y., Chan, C., Chew, L., Shih, P., Lee, C., & Chao, H. (2012). Meteorological factors and ambient bacterial levels in a subtropical urban environment. International Journal of Biometeorology, 56(6), 1001–1009.

    Google Scholar 

  • Wang, W., Ma, Y., Ma, X., Wu, F., Ma, X., An, L., et al. (2010). Seasonal variations of airborne bacteria in the Mogao Grottoes, Dunhuang, China. International Biodeterioration & Biodegradation, 64(4), 309–315.

    CAS  Google Scholar 

  • Xu, W. B., Qi, J. H., Jin, C., Gao, D. M., Li, M. F., Li, L., et al. (2011). Concentration distribution of bioaerosol in summer and autumn in the Qingdao coastal region. Environmental Science, 32(1), 9–17. (in Chinese).

    Google Scholar 

  • Xie, Z., Li, Y., Lu, R., Li, W., Fan, C., Liu, P., et al. (2018). Characteristics of total airborne microbes at various air quality levels. Journal of Aerosol Science, 116, 57–65.

    CAS  Google Scholar 

  • Zhao, Y., & Peng, C. (2015). Air microbial aerosol and human health. Cultural Geography., 22, 207. (in Chinese).

    Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (NSFC) under Grant No. 41775148 and the Fundamental Research Funds for the Central Universities (No. 201762006).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dahai Zhang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Y., Qi, J., Han, C. et al. Microbial characteristics of culturable fungi and bacteria in aerosol particles of a coastal region. Aerobiologia 36, 507–525 (2020). https://doi.org/10.1007/s10453-020-09648-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10453-020-09648-6

Keywords

Navigation