Microbial Ecology

, Volume 64, Issue 4, pp 973–985 | Cite as

Free Tropospheric Transport of Microorganisms from Asia to North America

  • David J. Smith
  • Daniel A. Jaffe
  • Michele N. Birmele
  • Dale W. Griffin
  • Andrew C. Schuerger
  • Jonathan Hee
  • Michael S. Roberts
Environmental Microbiology


Microorganisms are abundant in the troposphere and can be transported vast distances on prevailing winds. This study measures the abundance and diversity of airborne bacteria and fungi sampled at the Mt. Bachelor Observatory (located 2.7 km above sea level in North America) where incoming free tropospheric air routinely arrives from distant sources across the Pacific Ocean, including Asia. Overall deoxyribonucleic acid (DNA) concentrations for microorganisms in the free troposphere, derived from quantitative polymerase chain reaction assays, averaged 4.94 × 10−5 ng DNA m−3 for bacteria and 4.77 × 10−3 ng DNA m−3 for fungi. Aerosols occasionally corresponded with microbial abundance, most often in the springtime. Viable cells were recovered from 27.4 % of bacterial and 47.6 % of fungal samples (N = 124), with 49 different species identified by ribosomal DNA gene sequencing. The number of microbial isolates rose significantly above baseline values on 22–23 April 2011 and 13–15 May 2011. Both events were analyzed in detail, revealing distinct free tropospheric chemistries (e.g., low water vapor, high aerosols, carbon monoxide, and ozone) useful for ruling out boundary layer contamination. Kinematic back trajectory modeling suggested air from these events probably originated near China or Japan. Even after traveling for 10 days across the Pacific Ocean in the free troposphere, diverse and viable microbial populations, including presumptive plant pathogens Alternaria infectoria and Chaetomium globosum, were detected in Asian air samples. Establishing a connection between the intercontinental transport of microorganisms and specific diseases in North America will require follow-up investigations on both sides of the Pacific Ocean.


Microbial Abundance Free Troposphere Brevibacillus Airborne Bacterium Microbial Concentration 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Research funding was provided by the National Science Foundation (NSF) Integrative Graduate Education and Research Traineeship (IGERT) program at the University of Washington (UW) Graduate Program in Astrobiology, the National Geographic Society/Waitt Grants Program (W177-11), the NASA Astrobiology Institute Director's Discretionary Fund, the Washington NASA Space Grant Consortium, and the UW Biology Department (Sargent Award). The Mt. Bachelor Observatory atmospheric chemistry measurements were funded by NSF Grant ATM-0724327. Critical sampling support was made possible by Bryan Hicks, Patrick Ball, Carol Higginbotham, Tom Lomax, and the staff at Mt. Bachelor Ski Resort. The authors are grateful to Victoria Long, Clara Wright, and Phil Howard (NASA KSC) for assistance with SEM imaging and John Catechis, Gerard Newsham, and Martin Hayes (NASA KSC) for help with sequencing. We would also like to thank Ray Wheeler (NASA KSC) and the anonymous manuscript reviewers for their time and feedback. Any use of trade names is for descriptive purposes only and does not imply endorsement by the U.S. Government.


  1. 1.
    Anderson SM, Johnsen K, Sørensen J, Nielsen P, Jacobsen CS (2000) Pseudomonas frederiksbergensis sp. nov., isolated from soil at a coal gasification site. Int J Syst Evol Microbiol 50:1957–1964CrossRefGoogle Scholar
  2. 2.
    Ariya PA, Sun J, Eltouny NA, Hudson ED, Hayes CT, Kos G (2009) Physical and chemical characterization of bioaerosols – Implications for nucleation processes. Int Rev Phys Chem 28(1):1–32CrossRefGoogle Scholar
  3. 3.
    Aspiroz C, Moreno LA, Rezusta A, Rubio C (1999) Differentiation of three biotypes of Malassezia species on human normal skin. Mycopathologia 145:69–74PubMedCrossRefGoogle Scholar
  4. 4.
    Baek SH, Im WT, Oh HW, Lee JS, Oh HM, Lee ST (2006) Brevibacillus ginsengisoli sp. nov., a denitrifying bacterium isolated from soil of a ginseng field. Int J Syst Evol Microbiol 56:2665–2669PubMedCrossRefGoogle Scholar
  5. 5.
    Betzer PR, Carder KL, Duce RA et al (1989) Long-range transport of giant mineral aerosol particles. Nature 336:568–571CrossRefGoogle Scholar
  6. 6.
    Bovallius A, Roffey R, Henningson E (1980) Long-range transmission of bacteria. Ann N Y Acad Sci 353:186–200PubMedCrossRefGoogle Scholar
  7. 7.
    Brown JKM, Hovmøller MS (2002) Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297:537–541PubMedCrossRefGoogle Scholar
  8. 8.
    Burrows SM, Elbert W, Lawrence MG, Pöschl U (2009) Bacteria in the global atmosphere—part 1: review and synthesis of literature data for different ecosystems. Atmos Chem Phys 9:9263–9280CrossRefGoogle Scholar
  9. 9.
    Burrows SM, Butler T, Jöckel P, Tost H, Kerkweg A, Pöschl U, Lawrence MG (2009) Bacteria in the global atmosphere—part 2: modeling of emissions and transport between different ecosystems. Atmos Chem Phys 9:9281–9297CrossRefGoogle Scholar
  10. 10.
    Dobson CM, Ellison GB, Tuck AF, Vaida V (2000) Atmospheric aerosols as prebiotic chemical reactors. PNAS 97(22):11864–11868PubMedCrossRefGoogle Scholar
  11. 11.
    Draxler RR, Rolph GD (2003) HYSPLIT (HYbrid Single-Particle Lagrangian Integrated Trajectory). NOAA Air Resources Laboratory READY Website. http://www.arl.noaa.gov/ready/hysplit4.html. Accessed 22 February 2012
  12. 12.
    Elo S, Suominen I, Kämpfer P et al (2001) Paenibacillus borealis sp. nov., a nitrogen-fixing species isolated from spruce forest humus in Finland. Int J Syst Evol Microbiol 51:535–545PubMedGoogle Scholar
  13. 13.
    Fahlgren C, Hagström A, Nilsson D, Zweifel UL (2010) Annual variations in the diversity, viability, and origin of airborne bacteria. Appl Environ Microbiol 76(9):3015–3025PubMedCrossRefGoogle Scholar
  14. 14.
    Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71(7):4117–4120PubMedCrossRefGoogle Scholar
  15. 15.
    Fischer EV, Hsu NC, Jaffe DA, Jeong MJ, Gong SL (2009) A decade of dust: Asian dust and springtime aerosol load in the U.S. Pacific Northwest. Geophys Res Lett 36(3):L03821CrossRefGoogle Scholar
  16. 16.
    Fischer EV, Jaffe DA, Weatherhead EC (2011) Free tropospheric peroxyacetyl nitrate (PAN) and ozone at Mount Bachelor: potential causes of variability and timescale for trend detection. Atmos Chem Phys 11:5641–5654CrossRefGoogle Scholar
  17. 17.
    Fröhlich-Nowoisky J, Pickersgill DA, Després VR, Pöschl U (2009) High diversity of fungi in air particulate matter. PNAS 106(31):12814–12819PubMedCrossRefGoogle Scholar
  18. 18.
    Gadkar V, Rillig MC (2005) Application of Phi29 DNA polymerase mediated whole genome amplification on single spores of arbuscular mycorrhizal (AM) fungi. FEMS Microbiol Lett 242:65–71PubMedCrossRefGoogle Scholar
  19. 19.
    Gillespie DE, Rondon MR, Williamson LL, Handelsman J (2005) Metagenomic libraries from uncultured microorganisms. In: Osborn M, Smith C (eds) Molecular microbial ecology, Routledge. Taylor and Francis Group, Florence, pp 261–280Google Scholar
  20. 20.
    Griffin DW (2007) Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clin Microbiol Rev 20(3):459–477PubMedCrossRefGoogle Scholar
  21. 21.
    Griffin DW, Gonzalez C, Teigell N, Petrosky T, Northrup DE, Lyles M (2011) Observations on the use of membrane filtration and liquid impingement to collect airborne microorganisms in various atmospheric environments. Aerobiologia 27(1):25–35CrossRefGoogle Scholar
  22. 22.
    Hammond GW, Raddatz RL, Gelskey DE (1989) Impact of atmospheric dispersion and transport of viral aerosols on the epidemiology of influenza. Clin Infect Dis 11(3):494–497CrossRefGoogle Scholar
  23. 23.
    Hara K, Zhang D (2012) Bacterial abundance and viability in long-range transported dust. Atmos Environ 47:20–25CrossRefGoogle Scholar
  24. 24.
    Horneck G, Klaus DM, Mancinelli RL (2010) Space microbiology. Microbiol Mol Biol Rev 74(1):121–156PubMedCrossRefGoogle Scholar
  25. 25.
    Hospodsky D, Yamamoto N, Peccia J (2010) Accuracy, precision, and method detection limits of quantitative PCR for airborne bacteria and fungi. Appl Environ Microbiol 76(21):7004–7012PubMedCrossRefGoogle Scholar
  26. 26.
    Hua NP, Kobayashi F, Iwasaka Y, Shi GY, Naganuma T (2007) Detailed identification of desert-originated bacteria carried by Asian dust storms to Japan. Aerobiologia 23:291–298CrossRefGoogle Scholar
  27. 27.
    Jaffe D, McKendry I, Anderson T, Price H (2003) Six ‘new’ episodes of trans-Pacific transport of air pollutants. Atmos Environ 37:391–404CrossRefGoogle Scholar
  28. 28.
    Jaffe D, Prestbo E, Swartzendruber P et al (2005) Export of atmospheric mercury from Asia. Atmos Environ 39:3029–3038CrossRefGoogle Scholar
  29. 29.
    Jeon EM, Kim HJ, Jung K et al (2011) Impact of Asian dust events on airborne bacterial community assessed by molecular analyses. Atmos Environ 45:4313–4321CrossRefGoogle Scholar
  30. 30.
    Johnston GC, Young IE (1972) Variability of DNA content in individual cells of Bacillus. Nature 238:164–166CrossRefGoogle Scholar
  31. 31.
    Kellogg CA, Griffin DW (2006) Aerobiology and the global transport of desert dust. Trends Ecol Evol 21(11):638–644PubMedCrossRefGoogle Scholar
  32. 32.
    Lacey ME, West JS (2006) The Air Spora – A Manual for catching and identifying airborne biological particles. Springer, DordrechtGoogle Scholar
  33. 33.
    Maki T, Susuki S, Kobayashi F et al (2008) Phylogenetic diversity and vertical distribution of a halobacterial community in the atmosphere of an Asian dust (KOSA) source region, Dunhuang City. Air Qual Atmos Health 1:81–89CrossRefGoogle Scholar
  34. 34.
    Maki T, Susuki S, Kobayashi F et al (2010) Phylogenetic analysis of atmospheric halotolerant bacterial communities at high altitude in an Asian dust (KOSA) arrival region, Suzu City. Sci Total Environ 408:4556–4562PubMedCrossRefGoogle Scholar
  35. 35.
    Martiny JBH, Bohannan BJM, Brown JH et al (2006) Microbial biogeography: putting microorganisms on the map. Nature 4:102–112Google Scholar
  36. 36.
    Milgroom MG, Wang K, Zhou Y, Kaneko S (1996) Intercontinental population structure of the chestnut blight fungus, Cryphonectria parasitica. Mycologia 88(2):179–190CrossRefGoogle Scholar
  37. 37.
    Mims SA, Mims FM III (2004) Fungal spores are transported long distances in smoke from biomass fires. Atmos Environ 38:651–655CrossRefGoogle Scholar
  38. 38.
    Pearce DA, Bridge PD, Hughes KA et al (2009) Microorganisms in the atmosphere over Antarctica. FEMS Microbiol Ecol 69:143–157PubMedCrossRefGoogle Scholar
  39. 39.
    Prospero JM, Blades E, Mathison G, Naidu R (2005) Interhemispheric transport of viable fungi and bacteria from Africa to the Caribbean with soil dust. Aerobiologia 21:1–19CrossRefGoogle Scholar
  40. 40.
    Reidmiller DR, Jaffe DA, Fischer EV, Finley B (2010) Nitrogen oxides in the boundary layer and free troposphere at the Mt Bachelor Observatory. Atmos Chem Phys 10:6043–6062CrossRefGoogle Scholar
  41. 41.
    Roberts MS, Nakamura LK, Cohan FM (1994) Bacillus mojavensis sp. nov., distinguishable from Bacillus subtilis by sexual isolation, divergence in DNA sequence, and differences in fatty acid composition. Int J Syst Bacteriol 44(2):256–264PubMedCrossRefGoogle Scholar
  42. 42.
    Roberts MS, Nakamura LK, Cohan FM (1996) Bacillus vallismortis sp. nov., a close relative of Bacillus Subtilis, isolated from soil in Death Valley, California. Int J Syst Evol Microbiol 46(2):470–475Google Scholar
  43. 43.
    Shelton BG, Kirkland KH, Flanders D, Morris GK (2002) Profiles of airborne fungi in building and outdoor environments in the United States. Appl Environ Microbiol 68(4):1743–1753PubMedCrossRefGoogle Scholar
  44. 44.
    Shivaji S, Chaturvedi P, Suresh K et al (2006) Bacillus aerius sp. nov., Bacillus aerophilus sp. nov., Bacilus stratosphericus sp. nov. and Bacilus altitudinis sp. nov., isolated from cryogenic tubes used for collecting air samples from high altitudes. Int J Syst Evol Microbiol 56:1465–1473PubMedCrossRefGoogle Scholar
  45. 45.
    Simmer C, Volz PA (1993) The use of satellites to monitor global transmission of microbes. Int J Remote Sens 14(8):1447–1461CrossRefGoogle Scholar
  46. 46.
    Smith DJ, Griffin DW, Schuerger AC (2010) Stratospheric microbiology at 20 km over the Pacific Ocean. Aerobiologia 26(1):35–46CrossRefGoogle Scholar
  47. 47.
    Smith DJ, Griffin DW, McPeters RD, Ward PD, Schuerger AC (2011) Microbial survival in the stratosphere and implications for global dispersal. Aerobiologia 27:319–332CrossRefGoogle Scholar
  48. 48.
    Smith DJ, Griffin DW, Jaffe DA (2011) The high life: transport of microbes in the atmosphere. Eos 92(30):149–150CrossRefGoogle Scholar
  49. 49.
    Spooner B, Roberts P (2005) Fungi. Collins New Naturalist Library, LondonGoogle Scholar
  50. 50.
    Vaïtilingom M, Amato P, Sancelme M, Laj P, Leriche M, Delort AM (2010) Contribution of microbial activity to carbon chemistry in clouds. Appl Environ Microbiol 76(1):23–29PubMedCrossRefGoogle Scholar
  51. 51.
    VanCuren RA, Cahill TA (2002) Asian aerosols in North America: frequency and concentration of fine dust. J Geophys Res 107(D24):4804CrossRefGoogle Scholar
  52. 52.
    Wang W, Ma Y, Ma X, Wu F, Ma X, An L, Feng H (2011) Diversity and seasonal dynamics of airborne bacteria in the Mogao Grottoes, Dunhuang, China. Aerobiologia 28(1):27–38CrossRefGoogle Scholar
  53. 53.
    Weiss-Penzias P, Jaffe DA, Swartzendruber P et al (2006) Observations of Asian air pollution in the free troposphere at Mount Bachelor Observatory during the spring of 2004. J Geophys Res 111:D10304CrossRefGoogle Scholar
  54. 54.
    Womack AM, Bohannan BJM, Green JL (2010) Biodiversity and biogeography of the atmosphere. Phil Trans R Soc B 365:3645–3653PubMedCrossRefGoogle Scholar
  55. 55.
    Yamada M, Iwasaka Y, Kobayashi F, Zhang D (2010) Challenge of measuring bioaerosols at KOSA source areas: tethered balloon observation couples with individual particle analysis. Earozoru Kenkyu 25(1):13–22Google Scholar
  56. 56.
    Zhilina TN, Garnova ES, Tourova TP et al (2001) Amphibacillus fermentum sp. nov. and Amphibacillus tropicus sp. nov., new alkaliphic, facultatively anaerobic, saccharolytic bacilli from Lake Magadi. Microbiology 70(6):711–722CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • David J. Smith
    • 1
  • Daniel A. Jaffe
    • 2
  • Michele N. Birmele
    • 3
  • Dale W. Griffin
    • 4
  • Andrew C. Schuerger
    • 5
  • Jonathan Hee
    • 2
  • Michael S. Roberts
    • 3
  1. 1.Biology and AstrobiologyUniversity of WashingtonSeattleUSA
  2. 2.Department of Atmospheric SciencesUniversity of Washington-BothellBothellUSA
  3. 3.ESC Team QNANASAKennedy Space CenterUSA
  4. 4.U.S. Geological SurveyTallahasseeUSA
  5. 5.Department of Plant PathologyUniversity of FloridaGainesvilleUSA

Personalised recommendations