Survival of endospores of Bacillus subtilis on spacecraft surfaces under simulated martian environments: Implications for the forward contamination of Mars

Icarus

Volumn 165, Issue 2, 2003, Pages 253-276

  Schuerger, Andrew C ^a   Mancinelli, Rocco L ^b   Kern, Roger G ^c   Rothschild, Lynn J ^b   McKay, Christopher P ^b  

^a DYNAMAC CORPORATION   (United States)

^b NASA AMES RESEARCH CENTER   (United States)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Exobiology; Mars; Regoliths; Spectroscopy; Ultraviolet observations

Indexed keywords

EID: 0141873034     PISSN: 00191035     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0019-1035(03)00200-8     Document Type: Article

References (87)

1. Allen, C.C., Gooding, J.L., Jercinovic, M., Keil, K., 1981. Altered basaltic glass: a terrestrial analog to the soil of Mars. Icarus 45, 347-369.
2. Allen, C.C., Jager, K.M., Morris, R.V., Lindstrom, D.J., Lindstrom, M.M., Lockwood, J.P., 1998. JSC Mars-1: a martian soil simulant. In: Space 98: Proc. Conf. Amer. Soc. Civil Eng., pp. 469-476.
3. Appelbaum, J., Flood, D.J., 1990. Solar radiation on Mars. Solar Energy 45, 353-363.
4. Arvesen, J.C., Griffin, R.N., Pearson, B.D., 1969. Determination of extraterrestrial solar spectral irradiance from a research aircraft. Appl. Optics 8, 2215-2232.
5. Ashwood-Smith, M.J., Copeland, J., Wilcockson, J., 1968. Response of bacterial spores and Micrococcus radiodurans to ultraviolet irradiation at low temperatures. Nature 217, 337-338.
6. Badescu, V., 1998. Different strategies for the maximum solar radiation collection on Mars surface. Acta Astronaut. 43, 409-421.
7. Barengoltz, J.B., 1997. Microbiological Cleanliness of the Mars Pathfinder Spacecraft. In: Proc. of the 43rd Annual Technical Meeting "Contamination Control." Institute of Environmental Science, pp. 242-248.
8. Barth, C.A., Hord, C.W., Stewart, A.I., Lane, A.L., Dick, M.L., Anderson, G.P., 1973. Mariner 9 ultraviolet spectrometer experiment: seasonal variation of ozone on Mars. Science 179, 795-796.
9. Cockell, C.S., Catling, D.C., Davis, W.L., Snook, K., Kepner, R.L., Lee, P., McKay, C.P., 2000. The ultraviolet environment of Mars: biological implications past, present, and future. Icarus 146, 343-359.
10. Colburn, D.S., Pollack, J.B., Haberle, R.M., 1989. Diurnal variations in optical depth at Mars. Icarus 79, 159-189.
11. Crow, S., Smith III, J.H., 1995. Gas plasma sterilization: application of space-age technology. Infection Cont. Hosp. Epidem. 16, 483-487.
12. DeVincenzi, D.L., Race, M.S., Klein, H.P., 1998. Planetary protection, sample return missions and Mars exploration: history, status, and future needs. J. Geophys. Res. 103, 28577-28585.
13. Dose, K., Bieger-Dose, A., Kerz, O., Gill, M., 1991. DNA-strand breaks limit survival in extreme dryness. Origins Life Evol. Biosph. 21, 177-187.
14. Dose, K., Gill, M., 1995. DNA stability and survival of Bacillus subtilis spores in extreme dryness. Origins Life Evol. Biosph. 25, 277-293.
15. Dose, K., Klein, A., 1996. Response of Bacillus subtilis spores to dehydration and UV irradiation at extremely low temperatures. Origins Life Evol. Biosph. 26, 47-59.
16. Favero, M.S., 1971. Microbiologic assay of space hardware. Environ. Biol. Med. 1, 27-36.
17. Favero, M.S., Puleo, J.R., Marshall, J.H., Oxborrow, G.S., 1966. Comparative levels and types of microbial contamination detected in industrial clean rooms. Appl. Microbiol. 14, 539-551.
18. Foster, T.L., Winans, L., 1975. Psychrophilic microorganisms from areas associated with the Viking spacecraft. Appl. Microbiol. 30, 546-550.
19. Foster, T.L., Winans, L., Casey, R.C., Kirschner, L.E., 1978. Response of terrestrial microorganisms to a simulated martian environment. Appl. Environ. Microbiol. 35, 730-737.
20. Godwin, R., 2000. Mars: The NASA Mission Reports. Apogee Press, ON, Canada.
21. Golombek, M.P., Cook, R.A., Economou, T., Folkner, W.M., Haldermann, A.F.C., Kallemeyn, P.H., Knudsen, J., Manning, R.M., Moore, H.J., Parker, T.J., Rieder, R., Schofield, J.T., Smith, P.H., Vaughn, R.M., 1997. Overview of the Mars Pathfinder mission and assessment of landing site predictions. Science 278, 1743-1748.
22. Green, R.H., Taylor, D.M., Gustan, E.A., Fraser, S.J., Olson, R.L,, 1971. Survival of microorganisms in a simulated martian environment. Space Life Sci. 3, 12-24.
23. Haberle, R.M., McKay, C.P., Pollack, J.B., Gwynne, O.E., Atkinson, D.H., Appelbaum, J., Landis, G.A., Zurek, R.W., Flood, D.J., 1993. Atmospheric effects on the utility of solar power on Mars. In: Lewis, J.S., Matthews, M.S., Guerrieri, M.L. (Eds.), Resources of Near-Earth Space. Univ. of Arizona Press, Tucson, AZ, pp. 845-885.
24. Hagen, C.A., Hawrylewicz, E.J., Ehrlich, R., 1964. Survival of microorganisms in a simulated martian environment: I. Bacillus subtilis var. globigii. Appl. Microbiol. 12, 215-218.
25. Hagen, C.A., Hawrylewicz, E.J., Ehrlich, R., 1967. Survival of microorganisms in a simulated martian environment: II. Moisture and oxygen requirements for germination of Bacillus cereus and Bacillus subtilis var. niger spores. Appl. Microbiol. 15, 285-291.
26. Hagen, C.A., Hawrylewicz, E.J., Anderson, B.T., Cephus, M.L., 1970. Effect of ultraviolet on the survival of bacteria airborne in simulated martian dust clouds. Life Sci. Space Res. 8, 53-58.
27. Hawrylewicz, E.J., Gowdy, B., Ehrlich, R., 1962. Microorganisms under simulated martian environment. Nature 193, 497.
28. Hawrylewicz, E.J., Hagen, C.A., Ehrlich, R., 1964. Response of microorganisms to a simulated martian environment. Life Sci. Space Res. 3, 64-73.
29. Horneck, G., 1993. Responses of Bacillus subtilis spores to space environment: results from experiments in space. Origins Life Evol. Biosph. 23, 37-52.
30. Horneck, G., Bucker, H., Reitz, G., Requardt, H., Dose, K., Martens, K.D., Menningmann, H.D., Weber, P., 1984. Microorganisms in the space environment. Science 225, 226-228.
31. Horneck, G., Bucker, H., Reitz, G., 1994. Long-term survival of bacterial spores in space. Adv. Space Res. 14, 41-45.
32. Horneck, G., Eschweiler, U., Reitz, G., Wehner, J., Willimek, R., Strauch, K., 1995. Biological responses to space: results of the experiment "Exo-biological Unit" of ERA on Eurica I. Adv. Space Res. 16, 105-118.
33. Horneck, G., Rettberg, P., Reitz, G., Weimer, J., Eschweiler, U., Strauch, K., Panitz, C., Starke, V., Baumstark-Khan, C., 2001. Protection of bacterial spores in space: a contribution to the discussion of panspermia. Origins Life Evol. Biosph. 31, 527-547.
34. Imshenetsky, A.A., Abyzov, S.S., Voronov, G.T., Kuzjurina, L.A., Lysenko, S.V., Somikov, G.G., Fedorova, R.I., 1967. Exobiology and the effect of physical factors on microorganisms. Life Sci. Space Res. 5, 250-260.
35. Imshenetsky, A.A., Kouzyurina, L.A., Jakshina, V.M., 1973. On the multiplication of xerophilic microorganisms under simulated martian conditions. Life Sci. Space Res. 11, 63-66.
36. Jagger, J., 1985a. Far-UV killing, mutation and repair. In: Jagger, J. (Ed.), Solar-UV Actions on Living Cells. Praeger, New York, NY, pp. 10-31.
37. Jagger, J., 1985b. Near-UV killing, mutation and repair. In: Jagger, J. (Ed.), Solar-UV Actions On Living Cells. Praeger, New York, NY, pp. 32-58.
38. Jagger, J., 1985c. Near-UV sublethal actions. In: Jagger, J. (Ed.), Solar-UV Actions On Living Cells. Praeger, New York, NY, pp. 59-74.
39. James, P.B., Clancy, R.T., Lee, S.W., Martin, L.J., Singer, R.B., Smith, E., Kahn, R.A., Zurek, R.W., 1994. Monitoring Mars with the Hubble Space Telescope: 1990-1991 observations. Icarus 109, 79-101.
40. Kahn, R., Martin, T.Z., Zurek, R.W., Lee, S.W., 1992. The martian dust cycle. In: Kieffer, H.H., Jakosky, B.M., Snyder, CW., Mathews, M.S. (Eds.), Mars. Univ. of Arizona Press, Tucson, AZ, pp. 1017-1053.
41. Kieffer, H.H., Martin, T.Z., Peterfreund, A.R., Jakosky, B.M., Miner, E.D., Palluconi, F.D., 1977. Thermal and albedo mapping of Mars during the Viking primary mission. J. Geophys. Res. 82, 4249-4291.
42. Kieffer, H.H., Jakosky, B.M., Snyder, C.W., Mathews, M.S., 1992. Mars. Univ. of Arizona Press, Tucson, AZ.
43. Koch, A.L., 1994. Growth measurement. In: Gerhardt, P. (Ed.), Methods for General and Molecular Bacteriology. ASM Press, Washington, DC, USA, pp. 248-277.
44. Koike, J., Oshima, T., 1993. Planetary quarantine in the Solar System. Survival rates of some terrestrial organisms under simulated space conditions by proton irradiation. Acta Astronaut. 29, 629-632.
45. Koike, J., Oshima, T., Koike, K.A., Taguchi, H., Tanaka, K.L., Nishimura, K., Miyaji, M., 1992. Survival rates of some terrestrial microorganisms under simulated space conditions. Adv. Space Res. 12, 271-274.
46. Koike, J., Oshima, T., Kobayashi, K., Kawasaki, Y., 1995. Studies in the search for life on Mars. Adv. Space Res. 15, 211-214.
47. Koike, J., Hori, T., Katahira, Y., Koike, K.A., Tanaka, K.L., Kobayashi, K., Kawasaki, Y., 1996. Fundamental studies concerning planetary quarantine in space. Adv. Space Res. 18, 339-344.
48. Kooistra Jr., J.A., Mitchell, R.B., Strughold, H., 1957. The behavior of microorganisms under simulated martian environmental conditions. Astron. Soc. Pacific 70, 64-69.
49. Kuhn, W.R., Atreya, S.K., 1979. Solar radiation incident on the martian surface. J. Mol. Evol. 14, 57-64.
50. Landis, G.A., Jenkins, P.P., 2000. Measurement of the settling rate of atmospheric dust on Mars by the MAE instrument on Mars Pathfinder. J. Geophys. Res. 105, 1855-1857.
51. Lindberg, C., Horneck, G., 1991. Action spectra for survival and spore photoproduct formation of Bacillus subtilis irradiated with short-wavelength (200-300 nm) UV at atmospheric pressure and in vacuo. J. Photochem. Photobiol. B. 11, 69-80.
52. Lorenz, P.R., Hotchin, J., Markusen, A.S., Orlob, G.B., Hemenway, C.L., Hallgren, D.S., 1968. Survival of micro-organisms in space. Space Life Sci. 1, 118-130.
53. Mancinelli, R.L., Klovstad, M., 2000. Martian soil and UV radiation: microbial viability assessment on spacecraft surfaces. Planet. Space Sci. 48, 1093-1097.
54. Markiewicz, W.J., Sablotny, R.M., Keller, H.U., Thomas, N., Titov, D., Smith, P.H., 1999. Optical properties of the martian aerosols as derived from imager for Mars Pathfinder midday sky brightness data. J. Geophys. Res. 104, 9009-9017.
55. Morelli, F.A., Fehlner, F.P., Stembridge, C.H., 1962. Effect of ultra-high vacuum on Bacillus subtilis var. niger. Nature 196, 106-107.
56. Morris, R.V., Gooding, J.L., 1990. Origins of Marslike spectral and magnetic properties of a Hawaiian palagontic soil. J. Geophys. Res. 95, 14427-14434.
57. Morris, R.V., Golden, D.C., Bell III, J.F., Lauer, H.V., Adams, J.B., 1993. Pigmenting agents in martian soils: inferences from spectral, Mossbauer, and magnetic properties of nanophase and other iron oxides in Hawaiian palagonitic soil PN-9. Geochim. Cosmochim. Acta 57, 4597-4609.
58. Mutch, T.A., Binder, A.B., Huck, F.O., Levinthal, E.C., Liebers Jr., S., Morris, E.C., Patterson, W.R., Pollack, J.B., Sagan, C., Taylor, G.R., 1976. The surface of Mars: the view from the Viking 1 Lander. Science 193, 791-801.
59. Nicholson, W.L., Munakata, N., Horneck, G., Melosh, H.J., Setlow, P., 2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64, 548-572.
60. Owen, T., 1992. The Composition and early history of the atmosphere of Mars. In: Kieffer, H.H., Jakosky, B.M., Snyder, C.W., Mathews, M.S. (Eds.), Mars. Univ. of Arizona Press, Tucson, AZ, pp. 818-834.
61. Packer, E., Scher, S., Sagen, C., 1963. Biological contamination of Mars II. Cold and aridity as constraints on the survival of terrestrial microorganisms in simulated martian environments. Icarus 2, 293-316.
62. Patel, M.R., Zamecki, J.C., Catling, D.C., 2002. Ultraviolet radiation on the surface of Mars and the Beagle 2 UV sensor. Planet. Space Sci. 50, 915-927.
63. Pflug, I.J., 1971. Sterilization of space hardware. Environ. Biol. Med. 1, 63-81.
64. Pollack, J.B., Ockert-Bell, M.E., Shepard, M.K., 1995. Viking lander image analysis of martian atmospheric dust. J. Geophys. Res. 100, 5235-5250.
65. Puleo, J.R., Oxborrow, G.S., Fields, N.D., Herring, C.M., Smith, L.S., 1973. Microbiological profiles of four Apollo spacecraft. Appl. Microbiol. 26, 838-845.
66. Puleo, J.R., Fields, N.D., Bergstrom, S.L., Oxborrow, G.S., Stabekis, P.D., Koukol, R.C., 1977. Microbiological profiles of the Viking spacecraft. Appl. Environ. Microbiol. 33, 379-384.
67. Rambler, M.B., Margulis, L., 1980. Bacterial resistance to ultraviolet irradiation under anaerobiosis: implications for pre-Phanerozoic evolution. Science 210, 638-640.
68. Rieder, R., Economou, T., Wanke, H., Turkevich, A., Crisp, J.A., Brückner, J., Dreibus, G., McSween Jr., H.Y, 1997. The chemical composition of martian soil and rocks returned by the mobile alpha proton x-ray spectrometer: preliminary results from the x-ray mode. Science 278, 1771-1774.
69. Rummel, J.D., 2001. Planetary exploration in the time of astrobiology: protecting against biological contamination. Proc. Natl. Acad. Sci. 98, 2128-2131.
70. Ruschmeyer, O.R., Pflug, I.J., 1977. Determinations of microbial loads associated with microscopic-size particles of Kennedy Space Center soil. Life Sci. Space Res. 15, 59-63.
71. Sagan, C., Coleman, S., 1965. Spacecraft sterilization standards and contamination of Mars. Astronaut. Aeronaut. 3, 22-27.
72. Schofield, J.T., Barnes, JR., Crisp, D., Haberle, R.M., Larsen, S., Magalhaes, J.A., Murphy, J.R., Seiff, A., Wilson, G., 1997. The Mars Pathfinder atmospheric structure investigation/meteorology (ASI/MET) experiment. Science 278, 1752-1758.
73. Seiff, A., Kirk, D.B., 1977. Structure of the atmosphere of Mars in summer at mid-latitudes. J. Geophys. Res. 82, 4364-4378.
74. Setlow, P., 1988. Resistance of bacterial spores to ultraviolet light. Comments Mol. Cell. Biophys. 5, 253-264.
75. Setlow, P., 1995. Mechanisms for the prevention of damage to DNA in spores of Bacillus species. Annu. Rev. Microbiol. 49, 29-54.
76. Slieman, T.A., Nicholson, W.L., 2001. Role of dipicolinic acid in survival of Bacillus subtilis spores exposed to artificial and solar UV radiation. Appl. Environ. Microbiol. 67, 1274-1279.
77. Smith, P.H., Lemmon, M.T., 1999. Opacity of the martian atmosphere measured by the imager for Mars Pathfinder. J. Geophys. Res. 104, 8975-8985.
78. Smith, P.H., Bell III, J.E, Bridges, N.T., Britt, D.T., Gaddis, L., Greeley, R., Keller, H.U., Herkenhoff, K., Jaumann, R., Johnson, J.R., Kirk, R.L., Lemmon, M.T., Maki, J.N., Malin, M.C., Murchie, S.L., Oberst, J., Parker, T.J., Reid, R.J., Sablotny, R.M., Soderblom, L.A., Stoker, C.R., Sullivan, R.J., Thomas, N., Tomasko, M.G., Ward, W., Wegryn, E., 1997. Results from the Mars Pathfinder camera. Science 278, 1758-1764.
79. Soffen, G.A., 1977. The Viking project. J. Geophys. Res. 82, 3959-3970.
80. Soffen, G.A., Snyder, C.W., 1976. The first Viking mission to Mars. Science 193, 759-766.
81. Taylor, G.R., 1974. Space microbiology. Ann. Rev. Microbiol. 28, 121-137.
82. Tomasko, M.G., Doose, L.R., Lemmon, M.T., Smith, P.H., Wegryn, E., 1999. Properties of dust in the martian atmosphere from the imager on Mars Pathfinder. J. Geophys. Res. 104, 8987-9007.
83. Venkateswaran, K., Satomi, M., Chung, S., Kern, R., Koukol, R., Basic, C., White, D., 2001. Molecular microbial diversity of a spacecraft assembly facility. System. Appl. Microbiol. 24, 311-320.
84. Venkateswaran, K., Hattori, N., La Duc, M.T., Kern, R., 2003. ATP as a biomarker of viable microorganisms in clean-room facilities. J. Microbiol. Methods 52, 367-377.
85. Weber, P., Greenberg, M., 1985. Can spores survive in interstellar space? Nature 316, 403-407.
86. 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. Appl. Environ. Microbiol. 62, 2221-2227.
87. Young, R.S., Deal, P.H., Bell III, J.F., Allen, J.L., 1964. Bacteria under simulated martian conditions. Life Sci. Space Res. 2, 105-111.