Resistance of bacillus subtilis spore DNA to lethal ionizing radiation damage relies primarily on spore core components and DNA repair, with minor effects of oxygen radical detoxification

Applied and Environmental Microbiology

Volumn 80, Issue 1, 2014, Pages 104-109

  Moeller, Ralf ^a   Raguse, Marina ^a   Reitz, Günther ^a   Okayasu, Ryuichi ^b   Li, Zuofeng ^c   Klein, Stuart ^c   Setlow, Peter ^d   Nicholson, Wayne L ^c  

^a GERMAN AEROSPACE CENTER DLR   (Germany)

^b NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^c UNIVERSITY OF FLORIDA   (United States)

^d UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS SUBTILIS SPORES; CATALASE ACTIVITY; CORE COMPONENTS; DIPICOLINIC ACIDS; NONHOMOLOGOUS END JOINING; OXIDATIVE STRESS RESPONSE; OXYGEN RADICAL; REACTIVE OXYGEN SPECIES;

DETOXIFICATION; DNA; IONIZING RADIATION; METAL IONS; OXYGEN; RADIATION DAMAGE;

RADIATION SHIELDING;

BACTERIUM; DETOXIFICATION; DNA; IONIZATION; ORGANIC ACID; OXYGEN; PROTEIN; RADICAL; SOLUBILIZATION;

BACTERIAL DNA; BACTERIAL PROTEIN; DIPICOLINIC ACID; PICOLINIC ACID DERIVATIVE; REACTIVE OXYGEN METABOLITE; SPORE SPECIFIC PROTEINS, BACILLUS; SPORE-SPECIFIC PROTEINS, BACILLUS; WATER;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL SPORE; DNA REPAIR; IONIZING RADIATION; METABOLISM; RADIATION EXPOSURE;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; DNA REPAIR; DNA, BACTERIAL; PICOLINIC ACIDS; RADIATION, IONIZING; REACTIVE OXYGEN SPECIES; SPORES, BACTERIAL; WATER;

EID: 84891131447     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.03136-13     Document Type: Article

References (47)

1. Blatchley ER, Meeusen A, Aronson AI, Brewster L. 2005. Inactivation of Bacillus spores by ultraviolet or gamma radiation. J. Environ. Eng. 131:1245-1252. http://dx.doi.org/10.1061/(ASCE)0733-9372(2005)131:9(1245).
2. Horneck G. 1994. HZE particle effects in space. Acta Astronaut. 11:749- 755.
3. Niebuhr SE, Dickson JS. 2003. Destruction of Bacillus anthracis strain Sterne 34F2 spores in postal envelopes by exposure to electron beam irradiation. Lett. Appl. Microbiol. 37:17-20. http://dx.doi.org/10.1046/j.1472-765X.2003.01337.x.
4. Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P. 2000. Resistance of bacterial endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64:548-572. http://dx.doi.org/10.1128/MMBR.64.3.548-572.2000.
5. Horneck G, Klaus DM, Mancinelli RL. 2010. Space microbiology. Microbiol. Mol. Biol. Rev. 74:121-156. http://dx.doi.org/10.1128/MMBR.00016-09.
6. Setlow P. 2006. Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J. Appl. Microbiol. 101:514-525. http://dx.doi.org/10.1111/j.1365-2672.2005.02736.x.
7. Setlow P. 2007. I will survive: DNA protection in bacterial spores. Trends Microbiol. 15:172-180. http://dx.doi.org/10.1016/j.tim.2007.02.004.
8. Cadet J, Delatour T, Douki T, Gasparutto D, Pouget JP, Ravanat JL, Sauvaigo S. 1999. Hydroxyl radicals and DNA base damage. Mutat. Res. 424:9-21.
9. Goodhead DT. 1994. Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int. J. Radiat. Biol. 65:7-17.
10. Hutchinson F. 1985. Chemical changes induced in DNA by ionizing radiation. Prog. Nucleic Acid Res. Mol. Biol. 32:115-154.
11. Hada M, Sutherland BM. 2006. Spectrum of complex DNA damages depends on the incident radiation. Radiat. Res. 165:223-230. http://dx.doi.org/10.1667/RR3498.1.
12. Sutherland BM, Bennett PV, Sidorkina O, Laval J. 2000. Clustered damages and total lesions induced in DNA by ionizing radiation: oxidized bases and strand breaks. Biochemistry 39:8026-8031. http://dx.doi.org/10.1021/bi9927989.
13. Lomax ME, Gulston MK, O'Neill P. 2002. Chemical aspects of clustered DNA damage induction by ionising radiation. Radiat. Prot. Dosimetry 99:63-68. http://dx.doi.org/10.1093/oxfordjournals.rpd.a006840.
14. Dianov GL, O'Neill P, Goodhead DT. 2001. Securing genome stability by orchestrating DNA repair: removal of radiation-induced clustered lesions in DNA. Bioessays 23:745-749. http://dx.doi.org/10.1002/bies.1104.
15. Yokoya A, Shikazono N, Fujii K, Urushibara A, Akamatsu K, Watanabe R. 2008. DNA damage induced by the direct effect of radiation. Radiat. Phys. Chem. 77:1280-1285. http://dx.doi.org/10.1016/j.radphyschem.2008.05.021.
16. Asaithamby A, Chen DJ. 2011. Mechanism of cluster DNA damage repair in response to high-atomic number and energy particles radiation. Mutat. Res. 711:87-99. http://dx.doi.org/10.1016/j.mrfmmm.2010.11.002.
17. Granger AC, Gaidamakova EK, Matrosova VY, Daly MJ, Setlow P. 2011. Effects of Mn and Fe levels on Bacillus subtilis spore resistance and effects of Mn2 , other divalent cations, orthophosphate, and dipicolinic acid on protein resistance to ionizing radiation. Appl. Environ. Microbiol. 77:32-40. http://dx.doi.org/10.1128/AEM.01965-10.
18. Leggett MJ, McDonnell G, Denyer SP, Setlow P, Maillard JY. 2012. Bacterial spore structures and their protective role in biocide resistance. J. Appl. Microbiol. 113:485-498. http://dx.doi.org/10.1111/j.1365-2672.2012.05336.x.
19. McKenney PT, Driks A, Eichenberger P. 2013. The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat. Rev. Microbiol. 11:33-44.
20. Bagyan I, Casillas-Martinez L, Setlow P. 1998. The katX gene, which codes for the catalase in spores of Bacillus subtilis, is a forespore-specific gene controlled by SigmaF, and KatX is essential for hydrogen peroxide resistance of the germinating spore. J. Bacteriol. 180:2057-2062.
21. Casillas-Martinez L, Setlow P. 1997. Alkyl hydroperoxide reductase, catalase, MrgA, and superoxide dismutase are not involved in resistance of Bacillus subtilis spores to heat or oxidizing agents. J. Bacteriol. 179:7420- 7425.
22. Popham DL, Sengupta S, Setlow P. 1995. Heat, hydrogen peroxide, and UV resistance of Bacillus subtilis spores with increased core water content and with or without major DNA-binding proteins. Appl. Environ. Microbiol. 61:3633-3638.
23. Moeller R, Setlow P, Reitz G, Nicholson WL. 2009. Roles of small, acidsoluble spore proteins and core water content in survival of Bacillus subtilis spores exposed to environmental solar UV radiation. Appl. Environ. Microbiol. 75:5202-5208. http://dx.doi.org/10.1128/AEM.00789-09.
24. Ibarra JR, Orozco AD, Rojas JA, López K, Setlow P, Yasbin RE, Pedraza-Reyes M. 2008. Role of the Nfo and ExoA apurinic/apyrimidinic endonucleases in repair of DNA damage during outgrowth of Bacillus subtilis spores. J. Bacteriol. 190:2031-2038. http://dx.doi.org/10.1128/JB.01625-07.
25. Wang ST, Setlow B, Conlon EM, Lyon JL, Imamura D, Sato T, Setlow P, Losick R, Eichenberger P. 2006. The forespore line of gene expression in Bacillus subtilis. J. Mol. Biol. 358:16-37. http://dx.doi.org/10.1016/j.jmb.2006.01.059.
26. Pitcher RS, Brissett NC, Doherty AJ. 2007. Nonhomologous end-joining in bacteria: a microbial perspective. Annu. Rev. Microbiol. 61:259-282. http://dx.doi.org/10.1146/annurev.micro.61.080706.093354.
27. Salas-Pacheco JM, Setlow B, Setlow P, Pedraza-Reyes M. 2005. Role of the Nfo (YqfS) and ExoA apurinic/apyrimidinic endonucleases in protecting Bacillus subtilis spores from DNA damage. J. Bacteriol. 187:7374- 7381. http://dx.doi.org/10.1128/JB.187.21.7374-7381.2005.
28. Setlow B, Setlow P. 1996. Role of DNA repair in Bacillus subtilis spore resistance. J. Bacteriol. 178:3486-3495.
29. Lenhart JS, Schroeder JW, Walsh BW, Simmons LA. 2012. DNA repair and genome maintenance in Bacillus subtilis. Microbiol. Mol. Biol. Rev. 76:530-564. http://dx.doi.org/10.1128/MMBR.05020-11.
30. Schaeffer P, Millet J, Aubert JP. 1965. Catabolic repression of bacterial sporulation. Proc. Natl. Acad. Sci. U. S. A. 45:704-711.
31. Nicholson WL, Setlow P. 1990. Sporulation, germination, and outgrowth, p 391-450. In Harwood CR, Cutting SM (ed), Molecular biological methods for Bacillus. J. Wiley and Sons, Sussex, England.
32. Moeller R, Stackebrandt E, Reitz G, Berger T, Rettberg P, Doherty AJ, Horneck G, Nicholson WL. 2007. Role of DNA repair by nonhomologous end joining (NHEJ) in Bacillus subtilis spore resistance to extreme dryness, mono- and polychromatic UV and ionizing radiation. J. Bacteriol. 189:3306-3311. http://dx.doi.org/10.1128/JB.00018-07.
33. Moeller R, Setlow P, Horneck G, Berger T, Reitz G, Rettberg P, Doherty AJ, Okayasu R, Nicholson WL. 2008. Roles of the major, small, acidsoluble spore proteins and spore-specific and universalDNArepair mechanisms in resistance of Bacillus subtilis spores to ionizing radiation from X-rays and high-energy charged-particle bombardment. J. Bacteriol. 190: 1134-1140. http://dx.doi.org/10.1128/JB.01644-07.
34. Okayasu R, Okada M, Okabe A, Noguchi M, Takakura K, Takahashi S. 2006. Repair of DNA damage induced by accelerated heavy ions in mammalian cells proficient and deficient in the non-homologous end-joining pathway. Radiat. Res. 165:59-67. http://dx.doi.org/10.1667/RR3489.1.
35. Moeller R, Reitz G, Li Z, Klein S, Nicholson WL. 2012. Multifactorial resistance of Bacillus subtilis spores to high-energy proton radiation: role of spore structural components and the homologous recombination and non-homologous end joining DNA repair pathways. Astrobiology 12: 1069-1077. http://dx.doi.org/10.1089/ast.2012.0890.
36. Su Z, Lopatiuk-Tirpak O, Zeidan O, Sruprisan SI, Meeks SL, Slopsema R, Flampouri S, Li Z. 2012. An experimental investigation into the effect of periodic motion on proton dosimetry using polymer gel dosimeters and a programmable motion platform. Phys. Med. Biol. 57:649-663. http://dx.doi.org/10.1088/0031-9155/57/3/649.
37. Setlow B, Setlow P. 1993. Binding of small, acid-soluble spore proteins to DNA plays a significant role in the resistance of Bacillus subtilis spores to hydrogen peroxide. Appl. Environ. Microbiol. 59:3418-3423.
38. Hackett RH, Setlow P. 1988. Properties of spores of Bacillus subtilis strains which lack the major small, acid-soluble protein. J. Bacteriol. 170: 1403-1404.
39. Magge A, Granger AC, Wahome PG, Setlow B, Vepachedu VR, Loshon CA, Peng L, Chen D, Li YQ, Setlow P. 2008. Role of dipicolinic acid in the germination, stability, and viability of spores of Bacillus subtilis. J. Bacteriol. 190:4798-4807. http://dx.doi.org/10.1128/JB.00477-08.
40. Loshon CA, Genest PC, Setlow B, Setlow P. 1999. Formaldehyde kills spores of Bacillus subtilis by DNA damage and small, acid-soluble spore proteins of the alpha/beta-type protect spores against thisDNAdamage. J. Appl. Microbiol. 87:8-14.
41. Nicholson WL, Moeller R, Team PROTECT, Horneck G. 2012. Transcriptomic responses of germinating Bacillus subtilis spores exposed to 1.5 years of space parameters and simulated martian conditions on the EXPOSE- E experiment PROTECT. Astrobiology 12:469-486. http://dx.doi.org/10.1089/ast.2011.0748.
42. Ayora S, Carrasco B, Cárdenas PP, César CE, Cañas C, Yadav T, Marchisone C, Alonso JC. 2011. Double-strand break repair in bacteria: a view from Bacillus subtilis. FEMS Microbiol. Rev. 35:1055-1081. http://dx.doi.org/10.1111/j.1574-6976.2011.00272.x.
43. Bolz NJ, Lenhart JS, Weindorf SC, Simmons LA. 2012. Residues in the N-terminal domain of MutL required for mismatch repair in Bacillus subtilis. J. Bacteriol. 194:5361-5367. http://dx.doi.org/10.1128/JB.01142-12.
44. Rivas-Castillo AM, Yasbin RE, Robleto E, Nicholson WL, Pedraza-Reyes M. 2010. Role of the Y-family DNA polymerases YqjH and YqjW in protecting sporulating Bacillus subtilis cells from DNA damage. Curr. Microbiol. 60:263-267. http://dx.doi.org/10.1007/s00284-009-9535-3.
45. Mason JM, Setlow P. 1986. Essential role of small, acid-soluble spore proteins in resistance of Bacillus subtilis spores to UV light. J. Bacteriol. 167:174-178.
46. Wuytack EY, Boven S, Michiels CW. 1998. Comparative study of pressure- induced germination of Bacillus subtilis spores at low and high pressures. Appl. Environ. Microbiol. 64:3220-3224.
47. Setlow B, Atluri S, Kitchel R, Koziol-Dube K, Setlow P. 2006. Role of dipicolinic acid in resistance and stability of spores of Bacillus subtilis with or without DNA-protective alpha/beta-type small acid-soluble proteins. J. Bacteriol. 188:3740-3747. http://dx.doi.org/10.1128/JB.00212-06.