• Lewis Cuthbertson
  • David A. PearceEmail author


The atmosphere presents one of the most challenging environments on Earth with extreme psychrophilic and oligotrophic conditions. Cloud temperatures are typically below 0 °C, and stratospheric temperatures have been measured as low as −100 °C, colder than any other environment in the biosphere. Despite these challenges, the diversity of microbial life in the atmosphere has been found to be high, with over 100 bacterial genera recorded. Viable bacteria have been found in the stratosphere at altitudes of 77 km and bacteria collected from cloud water have been shown to be capable of both growth and reproduction at 0 °C suggesting the existence of psychrophilic bioaerosols. The role that microorganisms perform in processes such as ice nucleation, cloud formation, nitrogen processing, and the degradation of organic carbon-based compounds is becoming progressively clearer. However, the lack of a consensus on the most suitable bioaerosol sampling techniques makes progress challenging. Hence, although aerobiological studies date back as far as the mid nineteenth century, our understanding of microbial life in the atmosphere is still relatively limited. As the importance of understanding microbial biogeography continues to grow, particularly with regard to biogeography, long-range atmospheric dispersal, human health, and agriculture, more research is required to better understand the functional role of psychrophiles in the atmosphere.


  1. Airy H (1874) Pollen-grains in the air. Nature 10(253):355CrossRefGoogle Scholar
  2. Alger AS (1999) Diatoms of the McMurdo dry valleys, Antarctica: a taxonomic appraisal including a detailed study of the genus Hantzschia. Thesis, University of MichiganGoogle Scholar
  3. Amato P, Hennebelle R, Magand O, Sancelme M, Delort AM, Barbante C, Boutron C, Ferrari C (2007) Bacterial characterization of the snow cover at Spitzberg, Svalbard. FEMS Microbiol Ecol 59(2):255–264CrossRefPubMedGoogle Scholar
  4. Andersen AA (1958) New sampler for the collection, sizing and enumeration of viable airborne particles. J Bacteriol 76(5):471–484PubMedPubMedCentralGoogle Scholar
  5. Andrewes CH, Glover RE (1941) Spread of infection from the respiratory tract of the ferret. I. Transmission of influenza A virus. Br J Exp Pathol 22(2):91–97PubMedCentralGoogle Scholar
  6. Ariya PA, Nepotchatykh O, Ignatova O, Amyot M (2002) Microbiological degradation of atmospheric organic compounds. Geophys Res Lett 29(22):34-1–34-4CrossRefGoogle Scholar
  7. Baas Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. W.P. Van Stockum & Zoon, Den HaagGoogle Scholar
  8. Barberán A, Ladau J, Leff JW, Pollard KS, Menninger H, Dunn RR, Fierer N (2015) Continental-scale distributions of dust-associated bacteria and fungi. Proc Natl Acad Sci 112(18):5756–5761CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bauer H, Kasper-Giebl A, Löflund M, Giebl H, Hitzenberger R, Zibuschka F, Puxbaum H (2002) The contribution of bacteria and fungal spores to the organic carbon content of cloud water, precipitation and aerosols. Atmos Res 64(1–4):109–119CrossRefGoogle Scholar
  10. Blanchard DC, Syzdek LD (1982) Water-to-air transfer and enrichment of bacteria in drops from bursting bubbles. Appl Environ Microbiol 43(5):1001–1005PubMedPubMedCentralGoogle Scholar
  11. Bottos EM, Woo AC, Zawar-Reza P, Pointing SB, Cary SC (2014) Airborne bacterial populations above desert soils of the McMurdo Dry Valleys, Antarctica. Microb Ecol 67(1):120–128CrossRefPubMedGoogle Scholar
  12. Bourdillon RB, Lidwell OM, Thomas JC (1941) A slit sampler for collecting and counting air-borne bacteria. J Hyg 41(2):197–224CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bowers RM, 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. ISME J 5(4):601–612CrossRefPubMedGoogle Scholar
  14. Bowers RM, McCubbin IB, Hallar AG, Fierer N (2012) Seasonal variability in airborne bacterial communities at a high-elevation site. Atmos Environ 50:41–49CrossRefGoogle Scholar
  15. Brodie EL, DeSantis TZ, Parker JP, Zubietta IX, Piceno YM, Andersen GL (2007) Urban aerosols harbor diverse and dynamic bacterial populations. Proc Natl Acad Sci U S A 104(1):299–304CrossRefPubMedGoogle Scholar
  16. Brown WA, Allison VD (1937) Infection of the air of scarlet-fever wards with Streptococcus pyogenes. J Hyg 37(1):1–13CrossRefPubMedPubMedCentralGoogle Scholar
  17. Burrows SM, Butler T, Jöckel P, Tost H, Kerkweg A, Pöschl U, Lawrence MG (2009a) Bacteria in the global atmosphere – Part 2: Modeling of emissions and transport between different ecosystems. Atmos Chem Phys 9(23):9281–9297CrossRefGoogle Scholar
  18. Burrows SM, Elbert W, Lawrence MG, Pöschl U (2009b) Bacteria in the global atmosphere – Part 1: Review and synthesis of literature data for different ecosystems. Atmos Chem Phys 9(23):9263–9280CrossRefGoogle Scholar
  19. Chen PS, Tsai FT, Lin CK, Yang CY, Chan CC, Young CY, Lee CH (2010) Ambient influenza and avian influenza virus during dust storm days and background days. Environ Health Perspect 118(9):1211–1216CrossRefPubMedPubMedCentralGoogle Scholar
  20. Deguillaume L, Leriche M, Amato P, Ariya PA, Delort AM, Pöschl U, Chaumerliac N, Bauer H, Flossmann AI, Morris CE (2008) Microbiology and atmospheric processes: chemical interactions of primary biological aerosols. Biogeosciences 5(4):1073–1084CrossRefGoogle Scholar
  21. Després VR, Huffman JA, Burrows SM, Hoose C, Safatov AS, Buryak G, Fröhlich-Nowoisky J, Elbert W, Andreae MO, Pöschl U, Jaenicke R (2012) Primary biological aerosol particles in the atmosphere: a review. Tellus Ser B Chem Phys Meteorol 64:15598CrossRefGoogle Scholar
  22. Dimmick RL, Straat PA, Wolochow H, Levin GV, Chatigny MA, Schrot JR (1975) Evidence for metabolic activity of airborne bacteria. J Aerosol Sci 6(6):387–393CrossRefGoogle Scholar
  23. Dong L, Qi J, Shao C, Zhong X, Gao D, Cao W, Gao J, Bai R, Long G, Chu C (2016) Concentration and size distribution of total airborne microbes in hazy and foggy weather. Sci Total Environ 541:1011–1018CrossRefPubMedGoogle Scholar
  24. Dyar HG (1894) XII.—On certain bacteria from the air of New York City. Ann N Y Acad Sci 8:322–380CrossRefGoogle Scholar
  25. Fahlgren C, Hagstrom A, Nilsson D, Zweifel UL (2010) Annual variations in the diversity, viability, and origin of airborne bacteria. Appl Environ Microbiol 76(9):3015–3025CrossRefPubMedPubMedCentralGoogle Scholar
  26. Fierer N (2008) Microbial biogeography: patterns in microbial diversity across space and time. In: Zengler K (ed) Accessing uncultivated microorganisms: from the environment to organisms and back. ASM Press, Washington, DC, pp 95–115CrossRefGoogle Scholar
  27. Finlay BJ, Clarke KJ (1999) Ubiquitous dispersal of microbial species. Nature 400(6747):828–828CrossRefGoogle Scholar
  28. Gallisai R, Peters F, Volpe G, Basart S, Baldasano JM (2014) Saharan dust deposition may affect phytoplankton growth in the Mediterranean Sea at ecological time scales. PLoS ONE 9(10):e110762CrossRefPubMedPubMedCentralGoogle Scholar
  29. Giddings SN, MacCready P, Hickey BM, Banas NS, Davis KA, Siedlecki SA, Trainer VL, Kudela RM, Pelland NA, Connolly TP (2014) Hindcasts of potential harmful algal bloom transport pathways on the Pacific Northwest coast. J Geophys Res Oceans 119(4):2439–2461CrossRefGoogle Scholar
  30. Griffin DW (2007) Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clin Microbiol Rev 20(3):459–477CrossRefPubMedPubMedCentralGoogle Scholar
  31. Griffin DW, Gonzalez C, Teigell N, Petrosky T, Northup 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
  32. Harding T, Jungblut AD, Lovejoy C, Vincent WF (2011) Microbes in high Arctic snow and implications for the cold biosphere. Appl Environ Microbiol 77(10):3234–3243CrossRefPubMedPubMedCentralGoogle Scholar
  33. Herbold CW, Lee CK, McDonald IR, Cary SC (2014) Evidence of global-scale aeolian dispersal and endemism in isolated geothermal microbial communities of Antarctica. Nat Commun 5:3875CrossRefPubMedGoogle Scholar
  34. Hill KA, Shepson PB, Galbavy ES, Anastasio C, Kourtev PS, Konopka A, Stirm BH (2007) Processing of atmospheric nitrogen by clouds above a forest environment. J Geophys Res 112:D11301CrossRefGoogle Scholar
  35. Hirst JM (1952) An automatic volumetric spore trap. Ann Appl Biol 39(2):257–265CrossRefGoogle Scholar
  36. Hughes KA, McCartney HA, Lachlan-cope TA, Pearce DA (2004) A preliminary study of airborne microbial biodiversity over peninsular Antarctica. Cell Mol Biol 50(5):537–542PubMedGoogle Scholar
  37. Imshenetsky AA, Lysenko SV, Kasakov GA, Ramkova NV (1977) Resistance of stratospheric and mesospheric micro-organisms to extreme factors. Life Sci Space Res 15:37–39PubMedGoogle Scholar
  38. Johansson E, Adhikari A, Reponen T, Yermakov M, Grinshpun SA (2011) Association between increased DNA mutational frequency and thermal inactivation of aerosolized Bacillus spores exposed to dry heat. Aerosol Sci Technol 45(3):376–381CrossRefGoogle Scholar
  39. Jones AM, Harrison RM (2004) The effects of meteorological factors on atmospheric bioaerosol concentrations – a review. Sci Total Environ 326(1–3):151–180CrossRefPubMedGoogle Scholar
  40. Joung YS, Ge Z, Buie CR (2017) Bioaerosol generation by raindrops on soil. Nat Commun 8:14668CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kochkina GA, Ivanushkina NE, Karasev SG, Gavrish EY, Gurina LV, Evtushenko LI, Spirina EV, Vorob’eva EA, Gilichinskii DA, Ozerskaya SM (2001) Survival of micromycetes and actinobacteria under conditions of long-term natural cryopreservation. Microbiology 70(3):356–364CrossRefGoogle Scholar
  42. Lighthart B, Shaffer BT (1994) Bacterial flux from chaparral into the atmosphere in mid-summer at a high desert location. Atmos Environ 28(7):1267–1274CrossRefGoogle Scholar
  43. Lovejoy C, Vincent WF, Bonilla S, Roy S, Martineau M-J, Terrado R, Potvin M, Massana R, Pedrós-Alió C (2007) Distribution, phylogeny, and growth of cold-adapted picoprasinophytes in Arctic seas. J Phycol 43(1):78–89CrossRefGoogle Scholar
  44. Lurie MB (1930) Experimental epidemiology of tuberculosis. J Exp Med 51(5):743CrossRefPubMedPubMedCentralGoogle Scholar
  45. Madsen AM, Zervas A, Tendal K, Nielsen JL (2015) Microbial diversity in bioaerosol samples causing ODTS compared to reference bioaerosol samples as measured using Illumina sequencing and MALDI-TOF. Environ Res 140:255–267CrossRefPubMedGoogle Scholar
  46. Margesin R, Miteva V (2011) Diversity and ecology of psychrophilic microorganisms. Res Microbiol 162(3):346–361CrossRefPubMedGoogle Scholar
  47. Marshall WA (1996) Aerial dispersal of lichen soredia in the maritime Antarctic. New Phytol 134(3):523–530CrossRefGoogle Scholar
  48. Marshall WA (1998) Aerial transport of keratinaceous substrate and distribution of the fungus Geomyces pannorum in Antarctic soils. Microb Ecol 36(2):212–219CrossRefPubMedGoogle Scholar
  49. Marshall WA, Chalmers MO (1997) Airborne dispersal of antarctic terrestrial algae and cyanobacteria. Ecography 20(6):585–594CrossRefGoogle Scholar
  50. Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, Morin PJ, Naeem S, Ovreas L, Reysenbach A-L, Smith VH, Staley JT (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4(2):102–112CrossRefPubMedGoogle Scholar
  51. Meier FC, Lindbergh CA (1935) Collecting micro-organisms from the Arctic atmosphere. Sci Monthly 40:5–20Google Scholar
  52. Moeller R, Setlow P, Reitz G, Nicholson WL (2009) Roles of small, acid-soluble spore proteins and core water content in survival of Bacillus subtilis spores exposed to environmental solar UV radiation. Appl Environ Microbiol 75(16):5202–5208CrossRefPubMedPubMedCentralGoogle Scholar
  53. Möhler O, DeMott PJ, Vali G, Levin Z (2007) Microbiology and atmospheric processes: the role of biological particles in cloud physics. Biogeosciences 4(6):1059–1071CrossRefGoogle Scholar
  54. Molesworth AM, Cuevas LE, Connor SJ, Morse AP, Thomson MC (2003) Environmental risk and meningitis epidemics in Africa. Emerg Infect Dis 9(10):1287–1293CrossRefPubMedPubMedCentralGoogle Scholar
  55. Møller AK, Søborg DA, Al-Soud WA, Sørensen SJ, Kroer N (2013) Bacterial community structure in High-Arctic snow and freshwater as revealed by pyrosequencing of 16S rRNA genes and cultivation. Polar Res 32:17390CrossRefGoogle Scholar
  56. Morris CE, Conen F, Alex Huffman J, Phillips V, Pöschl U, Sands DC (2014) Bioprecipitation: a feedback cycle linking Earth history, ecosystem dynamics and land use through biological ice nucleators in the atmosphere. Glob Change Biol 20(2):341–351CrossRefGoogle Scholar
  57. NASA (2013) Earth’s atmospheric layers. Accessed 8 Feb 2017
  58. Nonnenmann MW, Bextine B, Dowd SE, Gilmore K, Levin JL (2010) Culture-independent characterization of bacteria and fungi in a poultry bioaerosol using pyrosequencing: a new approach. J Occup Environ Hyg 7(12):693–699CrossRefPubMedGoogle Scholar
  59. Pasteur L (1860) Nouvelles expériences relatives aux générations dites spontanées. C R Acad Sci 51:348–359Google Scholar
  60. Pearce DA, Bridge PD, Hughes KA, Sattler B, Psenner R, Russell NJ (2009) Microorganisms in the atmosphere over Antarctica. FEMS Microbiol Ecol 69(2):143–157CrossRefPubMedGoogle Scholar
  61. Pearce DA, Hughes KA, Lachlan-Cope T, Harangozo SA, Jones AE (2010) Biodiversity of air-borne microorganisms at Halley Station, Antarctica. Extremophiles 14(2):145–159CrossRefPubMedGoogle Scholar
  62. Pearce DA, Alekhina IA, Terauds A, Wilmotte A, Quesada A, Edwards A, Dommergue A, Sattler B, Adams BJ, Magalhaes C, Chu WL, Lau MC, Cary C, Smith DJ, Wall DH, Eguren G, Matcher G, Bradley JA, de Vera JP, Elster J, Hughes KA, Cuthbertson L, Benning LG, Gunde-Cimerman N, Convey P, Hong SG, Pointing SB, Pellizari VH, Vincent WF (2016) Aerobiology over Antarctica – a new initiative for atmospheric ecology. Front Microbiol 7:16CrossRefPubMedPubMedCentralGoogle Scholar
  63. Polunin N, Pady SM, Kelly CD (1947) Arctic aerobiology. Nature 160(4077):876–877CrossRefPubMedGoogle Scholar
  64. Sattler B, Puxbaum H, Psenner R (2001) Bacterial growth in supercooled cloud droplets. Geophys Res Lett 28(2):239–242CrossRefGoogle Scholar
  65. Seifried JS, Wichels A, Gerdts G (2015) Spatial distribution of marine airborne bacterial communities. Microbiology 4(3):475–490Google Scholar
  66. Smith DJ, Griffin DW, Jaffe DA (2011) The high life: transport of microbes in the atmosphere. EOS Trans Am Geophys Union 92(30):249–250CrossRefGoogle Scholar
  67. Smith DJ, Jaffe DA, Birmele MN, Griffin DW, Schuerger AC, Hee J, Roberts MS (2012) Free tropospheric transport of microorganisms from Asia to North America. Microb Ecol 64(4):973–985CrossRefPubMedGoogle Scholar
  68. Stewart FJ (2013) Where the genes flow. Nat Geosci 6(9):688–690CrossRefGoogle Scholar
  69. Vali G (1971) Quantitative evaluation of experimental results and the heterogeneous freezing nucleation of supercooled liquids. J Atmos Sci 28(3):402–409CrossRefGoogle Scholar
  70. Van Houdt R, De Boever P, Coninx I, Le Calvez C, Dicasillati R, Mahillon J, Mergeay M, Leys N (2009) Evaluation of the airborne bacterial population in the periodically confined Antarctic base Concordia. Microb Ecol 57(4):640–648CrossRefPubMedGoogle Scholar
  71. Vincent WF (2000) Evolutionary origins of Antarctic microbiota: invasion, selection and endemism. Antarct Sci 12(3):374–385CrossRefGoogle Scholar
  72. Vyverman W, Verleyen E, Wilmotte A, Hodgson DA, Willems A, Peeters K, Van de Vijver B, De Wever A, Leliaert F, Sabbe K (2010) Evidence for widespread endemism among Antarctic microorganisms. Polar Sci 4(2):103–113CrossRefGoogle Scholar
  73. Wainwright M, Wickramasinghe NC, Narlikar JV, Rajaratnam P (2003) Microorganisms cultured from stratospheric air samples obtained at 41 km. FEMS Microbiol Lett 218(1):161–165CrossRefPubMedGoogle Scholar
  74. Weber CF, Werth JT (2015) Is the lower atmosphere a readily accessible reservoir of culturable, antimicrobial compound-producing Actinomycetales? Front Microbiol 6:802CrossRefPubMedPubMedCentralGoogle Scholar
  75. Wells WF (1943) Bacteriologic procedures in sanitary air analysis: with special reference to air disinfection. J Bacteriol 46(6):549–557PubMedPubMedCentralGoogle Scholar
  76. Womack AM, Bohannan BJM, Green JL (2010) Biodiversity and biogeography of the atmosphere. Phil Trans Roy Soc London B: Biol Sci 365(1558):3645–3653CrossRefGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Applied Sciences, Faculty of Health and Life SciencesUniversity of Northumbria at NewcastleNewcastle upon TyneUK

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