Aerobiologia

, Volume 27, Issue 4, pp 319–332 | Cite as

Microbial survival in the stratosphere and implications for global dispersal

  • David J. Smith
  • Dale W. Griffin
  • Richard D. McPeters
  • Peter D. Ward
  • Andrew C. Schuerger
Original Paper

Abstract

Spores of Bacillus subtilis were exposed to a series of stratosphere simulations. In total, five distinct treatments measured the effect of reduced pressure, low temperature, high desiccation, and intense ultraviolet (UV) irradiation on stratosphere-isolated and ground-isolated B. subtilis strains. Environmental conditions were based on springtime data from a mid-latitude region of the lower stratosphere (20 km). Experimentally, each treatment consisted of the following independent or combined conditions: −70°C, 56 mb, 10–12% relative humidity and 0.00421, 5.11, and 54.64 W/m2 of UVC (200–280 nm), UVB (280–315 nm), UVA (315–400 nm), respectively. Bacteria were deposited on metal coupon surfaces in monolayers of ~1 × 106 spores and prepared with palagonite (particle size < 20 μm). After 6 h of exposure to the stratosphere environment, 99.9% of B. subtilis spores were killed due to UV irradiation. In contrast, temperature, desiccation, and pressure simulations without UV had no effect on spore viability up through 96 h. There were no differences in survival between the stratosphere-isolated versus ground-isolated B. subtilis strains. Inactivation of most bacteria in our simulation indicates that the stratosphere can be a critical barrier to long-distance microbial dispersal and that survival in the upper atmosphere may be constrained by UV irradiation.

Keywords

Stratosphere Natural selection Dispersal Spores Aerobiology 

Notes

Acknowledgments

Our research was supported by the National Science Foundation Integrative Graduate Education and Research Traineeship (IGERT) program at the University of Washington Graduate Program in Astrobiology, and the Cooperative Education Program at NASA Kennedy Space Center (KSC). Critical resources came from the U.S. Geological Survey (USGS), NASA Goddard Space Flight Center and the University of Florida. The authors are grateful to Paul Hintze (NASA KSC) for his assistance with SEM imaging and energy-dispersive X-ray spectrometry and to Phillip Metzger and Luke Roberson (NASA KSC) who helped generate the dust analog. We also acknowledge John Frederick (University of Chicago) for guidance during our research. Any use of trade names is for descriptive purposes only and does not imply endorsement by the US Government.

References

  1. Bates, D. R. (1984). Rayleigh scattering by air. Planetary and Space Sciences, 32(6), 785–790.CrossRefGoogle Scholar
  2. Benardini, J. N., Sawyer, J., Venkateswaran, K., & Nicholson, W. L. (2003). Spore UV and acceleration resistance of endolithic Bacillus pumilus and Bacillus subtilis isolates obtained from Sonoran Desert basalt: Implications for lithopanspermia. Astrobiology, 3(4), 709–717.CrossRefGoogle Scholar
  3. Betzer, P. R., et al. (1988). Long-range transport of giant mineral aerosol particles. Nature, 336, 568–571.CrossRefGoogle Scholar
  4. Blumthaler, M., Ambach, W., & Ellinger, R. (1997). Increase in solar UV radiation with altitude. Journal of Photochemistry and Photobiology, 39, 130–134.CrossRefGoogle Scholar
  5. Brasseur, G., & Solomon, S. (1986). Aeronomy of the middle atmosphere: Chemistry and physics of the stratosphere and mesosphere (pp. 1–30). Boston: Dordrecht.Google Scholar
  6. Broadwater, W. T., Hoehn, R. C., & King, P. H. (1973). Sensitivity of three selected bacterial species to ozone. Applied Microbiology, 26(3), 391–393.Google Scholar
  7. Carder, K. L., Steward, R. G., & Betzer, P. R. (1986). Dynamics and composition of particles from an aeolian input event to the Sargasso Sea. Journal of Geophysical Research, 91(D1), 1055–1066.CrossRefGoogle Scholar
  8. Daumont, D., Charbonnier, B. J., & Malicet, J. (1992). Ozone UV spectroscopy I: Absorption cross-sections at room temperature. Journal of Atmospheric Chemistry, 15, 145–155.CrossRefGoogle Scholar
  9. Deguillaume, L., et al. (2008). Microbiology and atmospheric processes: Chemical interactions of primary biological aerosols. Biogeosciences Discussions, 5, 841–870.CrossRefGoogle Scholar
  10. Dehel, T., Lorge, F., & Dickinson, M. (2008). Uplift of microorganisms by electric fields above thunderstorms. Journal of Electrostatics, 66, 463–466.CrossRefGoogle Scholar
  11. Dessler, A. (2000). The chemistry and physics of stratospheric ozone (pp. 1–16). San Diego: Academic Press. 117–126.Google Scholar
  12. Diaz, B., & Schulze-Makuch, D. (2006). Microbial survival rates of Escherichia coli and Deinococcus radiodurans under low temperature, low pressure, and UV-irradiation conditions, and their relevance to possible martian life. Astrobiology, 6(2), 332–347.CrossRefGoogle Scholar
  13. Dose, K., & Klein, A. (1996). Response of Bacillus subtilis spores to dehydration and UV irradiation at extremely low temperatures. Origins of Life and Evolution of the Biosphere, 26, 47–59.CrossRefGoogle Scholar
  14. Dose, K., et al. (2001). Survival of microorganisms under the extreme conditions of the Atacama Desert. Origins of Life and Evolution of the Biosphere, 31, 287–303.CrossRefGoogle Scholar
  15. Fajardo-Cavazos, P., & Nicholson, W. (2006). Bacillus endospores isolated from granite: Close molecular relationships to globally distributed Bacillus spp. from endolithic and extreme environments. Applied and Environmental Microbiology, 72(4), 2856–2863.CrossRefGoogle Scholar
  16. Ghosal, D., et al. (2005). How radiation kills cells: Survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress. FEMS Microbiology Reviews, 29, 361–375.Google Scholar
  17. Gierens, K., Schumann, U., Helten, M., Smit, H., & Marenco, A. (1999). A distribution law for relative humidity in the upper troposphere and lower stratosphere derived from three years of MOZAIC measurements. Annals of Geophysicae, 17, 1218–1226.CrossRefGoogle Scholar
  18. Griffin, D. W. (2004). Terrestrial microorganisms at an altitude of 20,000 m in earth’s atmosphere. Aerobiologia, 20, 135–140.CrossRefGoogle Scholar
  19. Griffin, D. W. (2008). 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.CrossRefGoogle Scholar
  20. Griffin, D. W. (2010). Observations on the use of membrane filtration and liquid impingement to collect airborne microorganisms in various atmospheric environments. Aerobiologia. doi:10.1007/s10453-010-9173-z.
  21. Harris, M. J., Wickramasinghe, N. C., Lloyd, D., Narlikar, J. V., Rajaratnam, P., Turner, M. P., et al. (2002). The detection of living cells in stratospheric samples. Proceedings of the Society of Photographic Instrumentation Engineers, 4495, 192–198.Google Scholar
  22. Horneck, G. (1993). Responses of Bacillus subtilis spores to the space environment: results from experiments in space. Origins of Life and Evolution of the Biosphere, 23, 37–52.CrossRefGoogle Scholar
  23. Horneck, G., Bücker, H., & Reitz, G. (1994). Long-term survival of bacterial spores in space. Advances in Space Research, 14, 41–45.CrossRefGoogle Scholar
  24. Imshenetsky, A. A., Lysenko, S. V., & Kasakov, G. A. (1978). Upper boundary of the biosphere. Applied and Environmental Microbiology, 35(1), 1–5.Google Scholar
  25. Imshenetsky, A. A., Lysenko, S. V., Kasakov, G. A., & Ramkova, N. V. (1977). Resistance of stratospheric and mesospheric micro-organisms to extreme factors. Life Sciences and Space Research, 15, 37–52.Google Scholar
  26. Imshenetsky, A. A., Lysenko, S. V., & Lach, S. P. (1979). Microorganisms of the upper layer of the atmosphere and the protective role of their cell pigments. Life Sciences and Space Research, 17, 105–110.Google Scholar
  27. Jacob, D. J. (1999). Introduction to atmospheric chemistry (pp. 1–23). Princeton: Princeton University Press. 42–71, 146–154.Google Scholar
  28. Junge, K., Eicken, H., Swanson, B. D., & Deming, J. W. (2006). Bacterial incorporation of leucine into protein down to −20°C with evidence for potential activity in sub-eutectic saline ice formations. Cryobiology, 52, 417–429.CrossRefGoogle Scholar
  29. Kellogg, C. A., & Griffin, D. W. (2006). Aerobiology and the global transport of desert dust. Trends in Ecology & Evolution, 21(11), 638–644.CrossRefGoogle Scholar
  30. Komanapalli, I. R., & Lau, B. H. S. (1998). Inactivation of bacteriophage λ, Escherichia coli, and Candida albicans by ozone. Applied Microbiology and Biotechnology, 49, 766–769.CrossRefGoogle Scholar
  31. Kondratyev, K. Y., Ivlev, L. S., Krapivin, V. F., & Varotsos, C. A. (Eds.). (2006). Atmospheric aerosol properties: Formation, processes and impacts (pp. 212–218). Chichester: Praxis Publishing, Ltd. 380, 425–448.Google Scholar
  32. Lysenko, S. V. (1980). Resistance of microorganisms of upper layers of the atmosphere to ultraviolet radiation and a high vacuum. Mikrobiologiia, 49(1), 175–177.Google Scholar
  33. Malicet, J., Daumont, D., Charbonnier, J., Parisse, C., Chakir, A., & Brion, J. (1995). Ozone UV spectroscopy II: Absorption cross-sections and temperature dependence. Journal of Atmospheric Chemistry, 21, 263–273.CrossRefGoogle Scholar
  34. Mancinelli, R. L., & Klovstad, M. (2000). Martian soil and UV radiation: Microbial viability assessment on spacecraft surfaces. Planetary and Space Sciences, 48, 1093–1097.CrossRefGoogle Scholar
  35. Martiny, J. B. H., et al. (2006). Microbial biogeography: Putting microorganisms on the map. Nature, 4, 102–112.Google Scholar
  36. McPeters, R. D., Heath, D. F., & Bhartia, P. K. (1984). Average ozone profiles for 1979 from the Nimbus-7 SBUV instrument. Journal of Geophysical Research, 89(4), 5199–5214.CrossRefGoogle Scholar
  37. McPeters, R. D., Krueger, A. J., Bhartia, P. K., Herman, J. R., Oakes, A., Ahmad, Z., et al. (1993). Nimbus-7 total ozone mapping spectrometer (TOMS) data products user’s guide. NASA reference publication 1323. Washington, DC: National Aeronautics and Space Administration.Google Scholar
  38. McPeters, R. D., Labow, G. J., & Logan, J. A. (2007). Ozone climatological profiles for satellite retrieval algorithms. Journal of Geophysical Research, 112, D05308.CrossRefGoogle Scholar
  39. Miyamoto-Shinohara, Y., Sukenobe, J., Imaizumi, T., & Nakahara, T. (2006). Survival curves for microbial species stored by freeze-drying. Cryobiology, 52, 27–32.CrossRefGoogle Scholar
  40. Narlikar, J. V., Lloyd, D., Wickramasinghe, N. C., Harris, M. J., Turner, M. P., Al-Mufti, S., et al. (2003). A balloon experiment to detect microorganisms in the outer space. Astrophysics and Space Science, 285(2), 555–562.CrossRefGoogle Scholar
  41. Nicholson, W. L., & Fajardo-Cavazos, P. (1997). DNA repair and the ultraviolet radiation resistance of bacterial spores: From the laboratory to the environment. Recent Research and Developments in Microbiology, 1, 125–140.Google Scholar
  42. Nicholson, W. L., & Law, J. F. (1999). Method for purification of bacterial endospores from soils: UV resistance of natural Sonoran Desert soil populations of Bacillus spp. with reference to B. subtilis strain 168. Journal of Microbiology Methods, 35, 13–21.CrossRefGoogle Scholar
  43. 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(3), 548–572.CrossRefGoogle Scholar
  44. Nicholson, W. L., et al. (2002). Bacterial endospores and their significance in stress resistance. Antonie van Leeuwenhoek, 81, 27–32.CrossRefGoogle Scholar
  45. Osman, S., et al. (2008). Effect of shadowing on survival of bacteria under conditions simulating the martian atmosphere and UV radiation. Applied and Environmental Microbiology, 74(4), 959–970.CrossRefGoogle Scholar
  46. Papke, R. T., & Ward, D. M. (2004). The importance of physical isolation to microbial diversification. FEMS Microbiological Ecology, 48, 293–303.CrossRefGoogle Scholar
  47. Randel, W. J., Park, M., Emmons, L., Kinnison, D., Bernath, P., Walker, K. A., et al. (2010). Asian monsoon transport of pollution to the stratosphere. Science, 238, 611–613.CrossRefGoogle Scholar
  48. Riesenman, P. J., & Nicholson, W. L. (2000). Role of spore coat layers in Bacillus subtilis spore resistance to hydrogen peroxide, artificial UV-C, UV-B, and solar UV radiation. Applied and Environmental Microbiology, 66(2), 620–626.CrossRefGoogle Scholar
  49. Saffary, R., et al. (2002). Microbial survival of space vacuum and extreme ultraviolet irradiation: Strain isolation and analysis during a rocket flight. FEMS Microbiology Letters, 215, 163–168.CrossRefGoogle Scholar
  50. Schmucki, D. A., & Philipona, R. (2002). Ultraviolet radiation in the Alps: The altitude effect. Optical Engineering, 41(12), 3090–3095.CrossRefGoogle Scholar
  51. Schuerger, A. C., Fajardo-Cavazos, P., Clausen, C. A., Moores, J. E., Smith, P. H., & Nicholson, W. L. (2008). Slow degradation of ATP in simulated martian environments suggests long residence times for the biosignature molecule on spacecraft surfaces on mars. Icarus, 194, 86–100.CrossRefGoogle Scholar
  52. Schuerger, A. C., Mancinelli, R. L., Kern, R. G., Rothschild, L. J., & McKay, C. P. (2003). Survival of endospores of Bacillus subtilis on spacecraft surfaces under simulated martian environments: Implications for the forward contamination of Mars. Icarus, 165, 253–376.CrossRefGoogle Scholar
  53. Schuerger, A. C., Richards, J. T., Newcombe, D. A., & Venkateswaran, K. (2006). Rapid inactivation of seven Bacillus spp. under simulated mars UV irradiation. Icarus, 181, 52–62.CrossRefGoogle Scholar
  54. Setlow, P. (1995). Mechanisms for the prevention of damage to DNA in spores of Bacillus species. Annual Reviews in Microbiology, 49, 29–54.CrossRefGoogle Scholar
  55. Setlow, P. (2001). Resistance of spores of Bacillus species to ultraviolet light. Environmental and Molecular Mutagenesis, 38, 97–104.CrossRefGoogle Scholar
  56. Setlow, P. (2007). I will survive: DNA protection in bacterial spores. Trends in Microbiology, 15(4), 172–180.CrossRefGoogle Scholar
  57. Shivaji, S., Chaturvedi, P., Begum, Z., Pindi, P. K., Manorama, R., Padmanaban, D. A., et al. (2009). Isolation of three novel bacterial strains, Janibacter hoylei sp. nov., Bacillus isronensis sp. nov. and Bacillus aryabhattai sp. nov. from cryotubes used for collecting air from upper atmosphere. International Journal of Systematic Evolution in Microbiology. doi:10.1099/ijs.0.002527-0.
  58. Shivaji, S., Chaturvedi, P., Suresh, K., Reddy, G. S. N., Dutt, C. B. S., Wainwright, M., et al. (2006). Bacillus aerius sp. nov., Bacillus aerophilus sp. nov., Bacillus stratosphericus sp. nov. and Bacillus altitudinis sp. nov., isolated from cryogenic tubes used for collecting air samples from high altitudes. International Journal of Systematic and Evolutionary Microbiology, 56, 1465–1473.CrossRefGoogle Scholar
  59. Slieman, T. A., & Nicholson, W. L. (2000). Artificial and solar UV radiation induces strand breaks and cyclobutane pyrimidine dimmers in Bacillus subtilis spore DNA. Applied and Environmental Microbiology, 66(1), 199–205.CrossRefGoogle Scholar
  60. Slieman, T. A., & Nicholson, W. L. (2001). Role of dipicolinic acid in survival of Bacillus subtilis spores exposed to artificial and solar UV radiation. Applied and Environmental Microbiology, 67(3), 1274–1279.CrossRefGoogle Scholar
  61. Smith, D. J., Griffin, D. W., & Schuerger, A. C. (2009). Stratospheric microbiology at 20 km over the Pacific Ocean. Aerobiologia, 26, 35–46.CrossRefGoogle Scholar
  62. Wainwright, M., Alharbi, S., & Wickramasinghe, N. C. (2006). How do microorganisms reach the stratosphere? International Journal of Astrobiology, 5(1), 13–15.CrossRefGoogle Scholar
  63. Wainwright, M., Wickramasinghe, N. C., Narlikar, J. V., & Rajaratnam, P. (2002). Microorganisms culture from stratospheric air samples obtained at 41 km. FEMS Microbiology Letters, 10778, 1–5.Google Scholar
  64. Wallace, J. M., & Hobbs, P. V. (2006). Atmospheric science: An introductory survey (2nd ed., pp. 1–21). New York: Academic Press. 113–198, 441–443.Google Scholar
  65. Xue, Y., & Nicholson, W. L. (1996). The two major spore DNA repair pathways, nucleotide excision repair and spore photoproduct lyase, are sufficient for the resistance of Bacillus subtilis spores to artificial UV-C and UV-B but not to solar radiation. Applied and Environmental Microbiology, 62(7), 2221–2227.Google Scholar
  66. Yang, Y., Itahashi, S., Yokobori, S., & Yamagishi, A. (2008a). UV-resistant bacteria isolated from upper troposphere and lower stratosphere. Biological Science in Space, 22, 18–25.CrossRefGoogle Scholar
  67. Yang, Y., Yokobori, S., Kawaguchi, J., Yamagami, T., Iijima, I., Izutsu, N., et al. (2008b). Investigation of cultivable microorganisms in the stratosphere collected by using a balloon in 2005. JAXA Research and Development Report, JAXA-RR-08-001, 35–42.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • David J. Smith
    • 1
  • Dale W. Griffin
    • 2
  • Richard D. McPeters
    • 3
  • Peter D. Ward
    • 1
  • Andrew C. Schuerger
    • 4
  1. 1.Department of Biology and Graduate Program in AstrobiologyUniversity of WashingtonSeattleUSA
  2. 2.U.S. Geological SurveyTallahasseeUSA
  3. 3.NASA Goddard Space Flight Center, Laboratory for AtmospheresGreenbeltUSA
  4. 4.Department of Plant Pathology, Space Life Sciences Laboratory, Kennedy Space CenterUniversity of FloridaGainesvilleUSA

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