Abstract
The influence of sample-collection-time on the recovery of culturable airborne microorganisms using a low-flow-rate membrane-filtration unit and a high-flow-rate liquid impinger were investigated. Differences in recoveries were investigated in four different atmospheric environments, one mid-oceanic at an altitude of ~10.0 m, one on a mountain top at an altitude of ~3,000.0 m, one at ~1.0 m altitude in Tallahassee, Florida, and one at ~1.0 m above ground in a subterranean-cave. Regarding use of membrane filtration, a common trend was observed: the shorter the collection period, the higher the recovery of culturable bacteria and fungi. These data also demonstrated that lower culturable counts were common in the more remote mid-oceanic and mountain-top atmospheric environments with bacteria, fungi, and total numbers averaging (by sample time or method categories) <3.0 colony-forming units (CFU) m−3. At the Florida and subterranean sites, the lowest average count noted was 3.5 bacteria CFU m−3, and the highest averaged 140.4 total CFU m−3. When atmospheric temperature allowed use, the high-volume liquid impinger utilized in this study resulted in much higher recoveries, as much as 10× greater in a number of the categories (bacterial, fungal, and total CFU). Together, these data illustrated that (1) the high-volume liquid impinger is clearly superior to membrane filtration for aeromicrobiology studies if start-up costs are not an issue and temperature permits use; (2) although membrane filtration is more cost friendly and has a ‘typically’ wider operational range, its limits include loss of cell viability with increased sample time and issues with effectively extracting nucleic acids for community-based analyses; (3) the ability to recover culturable microorganisms is limited in ‘extreme’ atmospheric environments and thus the use of a ‘limited’ methodology in these environments must be taken into account; and (4) the atmosphere culls, i.e., everything is not everywhere.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agranovski, I. E., Safatov, A. S., Borodulin, A. I., Pyankov, O. V., Petrishchenko, V. A., Sergeev, A. N., et al. (2004). Inactivation of viruses in bubbling processes utilized for personal bioaerosol monitoring. Applied and Environmental Microbiology, 70, 6963–6967.
Agranovski, I. E., Safatov, A. S., Pyankov, O. V., Sergeev, A. A., Sergeev, A. N., & Grinshpun, S. A. (2005). Long-term sampling of viable airborne viruses. Aerosol Science and Technology, 39, 912–918.
Bergman, W., Shinn, J., Lochner, R., Sawyer, S., Milanovich, F., Jr., & Mariella, R. (2005). High volume, low pressure drop, bioaerosol collector using a multi-slit virtual impactor. Journal of Aerosol Science, 36, 619–638.
Buttner, M. P., Willeke, K., & Grinshpun, S. A. (1997). Sampling and analysis of airborne microorganisms. In C. J. Hurst, G. R. Knudsen, M. J. McInerney, L. D. Stetzenbach, & M. V. Walter (Eds.), Manual of environmental microbiology (pp. 629–640). Washington, DC: American Society for Microbiology Press.
Dowd, S. E., & Maier, R. M. (2000). Aeromicrobiology. San Diego: Academic Press.
Dufrene, Y. F. (2000). Direct characterization of the physicochemical properties of fungal spores using functionalized AFM probes. Biophysical Journal, 78, 3286–3291.
Dytham, C. (1999). Choosing and using statistics, a biologist’s guide. Oxford: Blackwell Science.
Gorbushina, A. A., Kort, R., Schulte, A., Lazarus, D., Schnetger, B., Brumsack, H. J., et al. (2007). Life in Darwin’s dust: intercontinental transport and survival of microbes in the nineteenth century. Environmental Microbiology, 9, 2911–2922.
Gregory, P. H. (1961). The microbiology of the atmosphere. London: Leonard Hill Books Ltd.
Griffin, D. W. (2004). Terrestrial microorganisms at an altitude of 20,000 m in earth’s atmosphere. Aerobiologia, 20, 135–140.
Griffin, D. W. (2007a). Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clinical Microbiology Reviews, 20, 459–477.
Griffin, D. W. (2007b). Non-spore forming eubacteria isolated at an altitude of 20,000 m in earth’s atmosphere: extended incubation periods needed for culture-based assays. Aerobiologia, 24, 19–25.
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.
Griffin, D. W., Kellogg, C. A., Garrison, V. H., Lisle, J. T., Borden, T. C., & Shinn, E. A. (2003). African dust in the Caribbean atmosphere. Aerobiologia, 19, 143–157.
Griffin, D. W., Westphal, D. L., & Gray, M. A. (2006). Airborne microorganisms in the African desert dust corridor over the mid-Atlantic ridge, Ocean Drilling Program, Leg 209. Aerobiologia, 22, 211–226.
Honrath, R. E., Owen, R. C., Marti’n, M. V., Reid, J. S., Lapina, K., Fialho, P., et al. (2004). Regional and hemispheric impacts of anthropogenic and biomass burning emissions on summertime CO2 and O3 in the North Atlantic lower free troposphere. Journal of Geophysical Research, 109. doi:10.1029/2004JD005147.
Jensen, P. A., Lighthart, B., Mohr, A. J., & Shaffer, B. T. (1994). Instrumentation used with microbial bioaerosol. In B. Lighthart & A. J. Mohr (Eds.), Atmospheric microbial aerosols: theory and applications (pp. 226–284). New York, NY: Chapman and Hall.
Keleman, P. B., Kikawa, E., Miller, D. J., Abe, N., Bach, W., Carlson, R. L., et al. (2004). Leg 209 summary. In Proceedings of the Ocean Drilling Program, Initial Reports—Leg 209. College Station, TX: Ocean Drilling Program, pp. 1–139.
Kellogg, C. A., Griffin, D. W., Garrison, V. H., Peak, K. K., Royall, N., Smith, R. R., et al. (2004). Characterization of aerosolized bacteria and fungi from desert dust events in Mali, West Africa. Aerobiologia, 20, 99–110.
Koren, I., Kaufman, Y. J., Washington, R., Todd, M. C., Rudich, Y., Martins, J. V., et al. (2006). The Bodele depression: a single spot in the Sahara that provides most of the mineral dust to the Amazon forest. Environmental Research Letters, 1, 1–5.
Lin, X., Reponen, T., Willeke, K., Grinshpun, S. A., Foarde, K. K., & Ensor, D. S. (1999). Long-term sampling of airborne bacteria and fungi into a non-evaporating liquid. Atmospheric Environment, 33, 4291–4298.
Lin, X., Reponen, T., Willeke, K., Wang, Z., Grinshpun, S., & Trunov, M. (2000). Survival of airborne microorganisms during swirling aerosol collection. Aerosol Science and Technology, 32, 184–196.
Lin, X., Willeke, K., Ulevicius, V., & Grinshpun, S. (1997). Effect of sampling time on the collection efficiency of all-glass impingers. American Industrial Hygiene Association Journal, 58, 480–488.
Makino, S. I., Cheun, H. I., Watarai, M., Uchida, I., & Takeshi, K. (2001). Detection of anthrax spores from the air by real-time PCR. Letters in Applied Microbiology, 33, 237–240.
McFeters, G. A., Cameron, S. C., & LeChevallier, M. W. (1982). Influence of diluents, media, and membrane filter on detection of injured waterborne coliform bacteria. Applied and Environmental Microbiology, 43, 97–103.
Mohr, A. J. (1997). Fate and transport of microorganisms in air. Washington: ASM Press.
Pasteur, L. (1861) Memoire sur les corpuscles organises qui existent dans l’atmosphere. Examen de la doctrine des generations spontanees. Annales des Sciences Naturelles—Zoologie et Biologie Animale 4 e ser., 16, 5–98.
Prospero, J. M., Blades, E., Mathison, G., & Naidu, R. (2005). Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust. Aerobiologia, 21, 1–19.
Reasoner, D. J., & Geldreich, E. E. (1985). A new medium for the enumeration and subculture of bacteria from potable water. Applied and Environmental Microbiology, 49, 1–7.
Smith, D. J., Griffin, D. W., & Schuerger, A. C. (2009). Stratospheric microbiology at 20 km over the Pacific Ocean. Aerobiologia, 26(1), 35–46.
Terzieva, S., Donnelly, J., Ulevicius, V., Grinshpun, S. A., Willeke, K., Stelma, G. N., et al. (1996). Comparison of methods for detection and enumeration of airborne microorganisms collected by liquid impingement. Applied and Environmental Microbiology, 62, 2264–2272.
Tobin, R. S., Lomax, P., & Kushner, D. J. (1980). Comparison of nine brands of membrane filter and the most-probable-number methods for total coliform enumeration in sewage-contaminated drinking water. Applied and Environmental Microbiology, 40, 186–191.
Tyndall, J. (1882). Essays on the floating-matter of the air in relation to putrefaction and infection. New York and London: Johnson Reprint Corporation.
Wang, Z., & Reponen, T. (2001). Effect of sampling time and air humidity on the bioefficiency of filter samplers for bioaerosol collection. Journal of Aerosol Science, 32, 661–674.
Wolf, F. T. (1943). The microbiology of the upper air. Bulletin of the Torrey Botanical Club, 70, 1–14.
Yu, L., Wen, S., Li, J., Yang, W., Wang, J., Li, N., et al. (2009). Effects of different sampling solutions on the survival of bacteriophages in bubbling aeration. Aerobiologia. Online first: doi 10.1007/s10453-10009-19144-10454.
Acknowledgments
Appreciation is extended to Dr. Dan Jaffe of University of Washington at Bothell for support at Mount Bachelor Observatory and Dale Pate and Paul Burger of the U.S. National Park Service for assistance at Carlsbad Caverns National Park. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Griffin, D.W., Gonzalez, C., Teigell, N. et al. Observations on the use of membrane filtration and liquid impingement to collect airborne microorganisms in various atmospheric environments. Aerobiologia 27, 25–35 (2011). https://doi.org/10.1007/s10453-010-9173-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10453-010-9173-z