The Photochemistry of Unprotected DNA and DNA inside Bacillus subtilis Spores Exposed to Simulated Martian Surface Conditions of Atmospheric Composition, Temperature, Pressure, and Solar Radiation

Astrobiology

Volumn 18, Issue 4, 2018, Pages 393-402

  Nicholson, Wayne L ^a   Schuerger, Andrew C ^b   Douki, Thierry ^c  

^a KENNEDY SPACE CENTER   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIV GRENOBLE ALPES   (France)

Author keywords

Bacillus subtilis; DNA; Mars; Photochemistry; Spore; Ultraviolet

Indexed keywords

BACTERIAL DNA;

ASTRONOMY; ATMOSPHERE; BACILLUS SUBTILIS; BACTERIAL SPORE; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; PHOTOCHEMISTRY; PHYSIOLOGY; PRESSURE; SPACE; SUNLIGHT; TEMPERATURE;

ATMOSPHERE; BACILLUS SUBTILIS; DNA, BACTERIAL; EXTRATERRESTRIAL ENVIRONMENT; MARS; PHOTOCHEMICAL PROCESSES; PRESSURE; SPORES, BACTERIAL; SUNLIGHT; TEMPERATURE;

EID: 85045853259     PISSN: 15311074     EISSN: None     Source Type: Journal    
DOI: 10.1089/ast.2017.1721     Document Type: Article

References (65)

1. Alvarez, A., Khanna, M., Toranzos, G., and Stotzky, G. (1998) Amplification of DNA bound on clay minerals. Mol Ecol 7: 775-778.
2. Botta, O., Glavin, D. P., Kminek, G., and Bada, J. L. (2002) Relative amino acid concentrations as a signature for parent body processes of carbonaceous chondrites. Orig Life Evol Biosph 32:143-163.
3. Carr, C. E., Rowedder, H., Lui, C. S., Zlatkovsky, I., Papalias, C. W., Bolander, J., Myers, J. W., Bustillo, J., Rothberg, J. M., Zuber, M. T., and Ruvkun, G. (2013a) Radiation resistance of sequencing chips for in situ life detection. Astrobiology 13:560-569.
4. Carr, C. E., Rowedder, H., Vafadari, C., Lui, C. S., Cascio, E., Zuber, M. T., and Ruvkun, G. (2013b) Radiation resistance of biological reagents for in situ life detection. Astrobiology 13: 68-78.
5. Checinska, A., Probst, A. J., Vaishampayan, P., White, J. R., Kumar, D., Stepanov, V. G., Fox, G. E., Nilsson, H. R., Pierson, D. L., Perry, J., and Venkateswaran, K. (2015) Microbiomes of the dust particles collected from the International Space Station and spacecraft assembly facilities. Microbiome 3, doi:10. 1186/s40168-015-0116-3.
6. Cutting, S. M. and Vander Horn, P. B. (1990) Genetic analysis. In Molecular Biological Methods for Bacillus, edited by C. R. Harwood and S. M. Cutting, John Wiley and Sons, Sussex, UK, pp 27-74.
7. Donnellan, J. E., Jr. and Setlow, R. B. (1965) Thymine photoproducts but not thymine dimers are found in ultravioletirradiated bacterial spores. Science 149:308-310.
8. Douki, T. (2013) The variety of UV-induced pyrimidine dimeric photoproducts in DNA as shown by chromatographic quantification methods. Photochem Photobiol Sci 12:1286-1302.
9. Douki, T. and Cadet, J. (2003) Formation of the spore photoproduct and other dimeric lesions between adjacent pyrimidines in UVC-irradiated dry DNA. Photochem Photobiol Sci 2:433-436.
10. Douki, T., Laporte, G., and Cadet, J. (2003) Inter-strand photoproducts are produced in high yield within A-DNA exposed to UVC radiation. Nucleic Acids Res 31:3134-3142.
11. Douki, T., Setlow, B., and Setlow, P. (2005a) Effects of the binding of alpha/beta-type small, acid-soluble spore proteins on the photochemistry of DNA in spores of Bacillus subtilis and in vitro. Photochem Photobiol 81:163-169.
12. Douki, T., Setlow, B., and Setlow, P. (2005b) Photosensitization of DNA by dipicolinic acid, a major component of spores of Bacillus species. Photochem Photobiol Sci 4:591-597.
13. Ehrenfreund, P., Glavin, D. P., Botta, O., Cooper, G., and Bada, J. L. (2001) Extraterrestrial amino acids in Orgueil and Ivuna: tracing the parent body of Cl type carbonaceous chondrites. Proc Natl Acad Sci USA 98:2138-2141.
14. Fajardo-Cavazos, P., Schuerger, A., and Nicholson, W. (2007) Testing interplanetary transfer of bacteria between Earth and Mars as a result of natural impact phenomena and human spaceflight activities. Acta Astronaut 60:534-540.
15. Fajardo-Cavazos, P., Schuerger, A., and Nicholson, W. (2008) Persistence of biomarker ATP and ATP-generating capability in bacterial cells and spores contaminating spacecraft materials under earth conditions and in a simulated martian environment. Appl Enivron Microbiol 74:5159-5167.
16. Fajardo-Cavazos, P., Schuerger, A. C., and Nicholson, W. L. (2010) Exposure of DNA and Bacillus subtilis spores to simulated martian environments: use of quantitative PCR (qPCR) to measure inactivation rates of DNA to function as a template molecule. Astrobiology 10:403-411.
17. Friedberg, E. C., Walker, G. C., Siede, W., Wood, R. D., Schultz, R. A., and Ellenberger, T. (2006) DNA Repair and Mutagenesis, ASM Press, Washington, DC.
18. Glavin, D. P., Dworkin, J. P., and Sandford, S. A. (2008) Detection of cometary amines in samples returned by Stardust. Meteorit Planet Sci 43:399-413.
19. ISECG. (2013) The Global Exploration Roadmap, NASA Headquarters, Washington DC.
20. Isenbarger, T. A., Carr, C. E., Johnson, S. S., Finney, M., Church, G. M., Gilbert, W., Zuber, M. T., and Ruvkun, G. (2008) The most conserved genome segments for life detection on Earth and other planets. Orig Life Evol Biosph 38:517-533.
21. Johns, H. E., Rapaport, S. A., and DelbrÜck, M. (1962) Photochemistry of thymine dimers. J Mol Biol 4:104-114.
22. Kempf, M., Chen, F., Kern, R., and Venkateswaran, K. (2005) Recurrent isolation of hydrogen peroxide-resistant spores of Bacillus pumilus from a spacecraft assembly facility. Astrobiology 5:391-405.
23. Kieffer, H. H. (1976) Soil and surface temperatures at the Viking landing sites. Science 194:1344-1346.
24. La Duc, M., Nicholson, W., Kern, R., and Venkateswaran, K. (2003) Microbial characterization of the Mars Odyssey spacecraft and its encapsulation facility. Environ Microbiol 5:977-985.
25. La Duc, M., Kern, R., and Venkateswaran, K. (2004) Microbial monitoring of spacecraft and associated environments. Microb Ecol 47:150-158.
26. La Duc, M., Dekas, A., Osman, S., Moissl, C., Newcombe, D., and Venkateswaran, K. (2007) Isolation and characterization of bacteria capable of tolerating the extreme conditions of clean room environments. Appl Environ Microbiol 73:2600-2611.
27. Leggett, M. J., McDonnell, G., Denyer, S. P., Setlow, P., and Maillard, J. Y. (2012) Bacterial spore structures and their protective role in biocide resistance. J Appl Microbiol 113:485-498.
28. Lemaire, D. G. E. and Ruzsicska, B. P. (1993) Quantum yields and secondary photoreactions of the photoproducts of dTpdT, dTpdC and dTpdU. Photochem Photobiol 57:755-769.
29. Link, L., Sawyer, J., Venkateswaran, K., and Nicholson, W. (2004) Extreme spore UV resistance of Bacillus pumilus isolates obtained from an ultraclean spacecraft assembly facility. Microb Ecol 47:159-163.
30. Martins, Z., Botta, O., Fogel, M. L., Sephton, M. A., Glavin, D. P., Watson, J. S., Dworkin, J. P., Schwartz, A. W., and Ehrenfreund, P. (2008) Extraterrestrial nucleobases in the Murchison meteorite. Earth Planet Sci Lett 270:130-136.
31. Miller, J. H. (1972) Experiments in Molecular Genetics, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
32. Moeller, R., Douki, T., Cadet, J., Stackebrandt, E., Nicholson, W. L., Rettberg, P., Reitz, G., and Horneck, G. (2007) UVradiation-induced formation of DNA bipyrimidine photoproducts in Bacillus subtilis endospores and their repair during germination. Int Microbiol 10:39-46.
33. Moores, J. E., Smith, P. H., Tanner, R., Schuerger, A. C., and Venkateswaran, K. J. (2007) The shielding effect of smallscale martian surface geometry on ultraviolet flux. Icarus 192:417-433.
34. Morris, H. C., Monaco, L. A., Steele, A., and Wainwright, N. (2010) Setting a standard: the Limulus amebocyte lysate assay and the assessment of microbial contamination on spacecraft surfaces. Astrobiology 10:845-852.
35. NASA. (2014) 2014 Astrobiology Strategic Plan, NASA, Washington, DC.
36. National Research Council. (2006) Preventing the Forward Contamination of Mars, National Academies Press, Washington, DC.
37. National Research Council. (2007) An Astrobiology Strategy for the Exploration of Mars, National Academies Press, Washington, DC.
38. Nicholson, W., Schuerger, A., and Race, M. (2009) Migrating microbes and planetary protection. Trends Microbiol 17:389-392.
39. Nicholson, W. L. and Setlow, P. (1990) Sporulation, germination, and outgrowth. In Molecular Biological Methods for Bacillus, edited by C. R. Harwood and S. M. Cutting, John Wiley & Sons, New York, pp 391-450.
40. Nicholson, W. L., Munakata, N., Horneck, G., Melosh, H. J., and Setlow, P. (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64:548-572.
41. Nicholson, W. L., Schuerger, A. C., and Setlow, P. (2005) The solar UV environment and bacterial spore UV resistance: considerations for Earth-to-Mars transport by natural processes and human spaceflight. Mutat Res 571:249-264.
42. Owen, T. (1992) The composition and early history of the atmosphere of Mars. In Mars, edited by H. H. Keiffer, B. M. Jakosky, C. W. Snyder, and M. S. Matthews, University of Arizona Press, Tucson, AZ, pp 818-834.
43. Pizzarello, S., Williams, L. B., Lehman, J., Holland, G. P., and Yarger, J. L. (2011) Abundant ammonia in primitive asteroids and the case for a possible exobiology. Proc Natl Acad Sci USA 108:4303-4306.
44. Rahn, R. O. and Hosszu, J. L. (1969) Influence of relative humidity on the photochemistry of DNA films. Biochim Biophys Acta 190:126-131.
45. Rummel, J. (2001) Planetary exploration in the time of astrobiology: protecting against biological contamination. Proc Natl Acad Sci USA 98:2128-2131.
46. Rummel, J. D., Beaty, D. W., Jones, M. A., Bakermans, C., Barlow, N. G., Boston, P. J., Chevrier, V. F., Clark, B. C., de Vera, J. P., Gough, R. V., Hallsworth, J. E., Head, J. W., Hipkin, V. J., Kieft, T. L., McEwen, A. S., Mellon, M. T., Mikucki, J. A., Nicholson, W. L., Omelon, C. R., Peterson, R., Roden, E. E., Sherwood Lollar, B., Tanaka, K. L., Viola, D., and Wray, J. J. (2014) A new analysis of Mars ''Special Regions'': findings of the second MEPAG Special Regions Science Analysis Group (SR-SAG2). Astrobiology 14:887-968.
47. Sambrook, J. and Russell, D. W. (2001) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Schaeffer, P., Millet, J., and Aubert, J. P. (1965) Catabolic repression of bacterial sporulation. Proc Natl Acad Sci USA 54: 704-711.
49. Schuerger, A., Mancinelli, R., Kern, R., Rothschild, L., and McKay, C. (2003) Survival of endospores of Bacillus subtilis on spacecraft surfaces under simulated martian environments: implications for the forward contamination of Mars. Icarus 165:253-276.
50. Schuerger, A., Richards, J., Hintze, P., and Kern, R. (2005) Surface characteristics of spacecraft components affect the aggregation of microorganisms and may lead to different survival rates of bacteria on Mars landers. Astrobiology 5: 545-559.
51. Schuerger, A., Richards, J., Newcombe, D., and Venkateswaran, K. (2006) Rapid inactivation of seven Bacillus spp. under simulated Mars UV irradiation. Icarus 181:52-62.
52. Schuerger, A. C., Fajardo-Cavazos, P., Clausen, C. A., Moores, J. E., Smith, P. H., and 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.
53. Setlow, P. (2006) Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J Appl Microbiol 101:514-525.
54. Setlow, P. and Li, L. (2015) Photochemistry and photobiology of the spore photoproduct: a 50-year journey. Photochem Photobiol 91:1263-1290.
55. Sikorsky, J., Primerano, D., Fenger, T., and Denvir, J. (2004) Effect of DNA damage on PCR amplification efficiency with the relative threshold cycle method. Biochem Biophys Res Commun 323:823-830.
56. Slieman, T. and Nicholson, W. (2000) Artificial and solar UV radiation induces strand breaks and cyclobutane pyrimidine dimers in Bacillus subtilis spore DNA. Appl Environ Microbiol 66:199-205.
57. Slieman, T., Rebeil, R., and Nicholson, W. (2000) Spore photoproduct (SP) lyase from Bacillus subtilis specifically binds to and cleaves SP (5-thyminyl-5, 6-dihydrothymine) but not cyclobutane pyrimidine dimers in UV-irradiated DNA. J Bacteriol 182:6412-6417.
58. Smith, S. A., Benardini, J. N., III, Anderl, D., Ford, M., Wear, E., Schrader, M., Schubert, W., DeVeaux, L., Paszczynski, A., and Childers, S. E. (2017) Identification and characterization of early mission phase microorganisms residing on the Mars Science Laboratory and assessment of their potential to survive Mars-like conditions. Astrobiology 17:253-265.
59. Tauscher, C., Schuerger, A., and Nicholson, W. (2006) Survival and germinability of Bacillus subtilis spores exposed to simulated Mars solar radiation: implications for life detection and planetary protection. Astrobiology 6:592-605.
60. Taylor, J.-S. and Cohrs, M. P. (1987) DNA, light, and Dewar pyrimidones: the structure and biological significance of TpT3. J Am Chem Soc 109:2834-2835.
61. Taylor, J. S., Garrett, D. S., and Cohrs, M. P. (1988) Solutionstate structure of the Dewar pyrimidinone photoproduct of thymidylyl-(3'-5')-thymidine. Biochemistry 27:7206-7215.
62. ten Kate, I., Garry, J., Peeters, Z., Quinn, R., Foing, B., and Ehrenfreund, P. (2005) Amino acid photostability on the martian surface. Meteorit Planet Sci 40:1185-1193.
63. Tyrrell, R. M. (1978) Solar dosimetry with repair deficient bacterial spores: action spectra, photoproduct measurements, and comparison with other biological systems. Photochem Photobiol 27:571-579.
64. Venkateswaran, K., Satomi, M., Chung, S., Kern, R., Koukol, R., Basic, C., and White D. (2001) Molecular microbial diversity of a spacecraft assembly facility. Syst Appl Microbiol 24:311-320.
65. Venkateswaran, K., Hattori, N., La Duc, M., and Kern, R. (2003) ATP as a biomarker of viable microorganisms in clean-room facilities. J Microbiol Methods 52:367-377.