Journal of Microbiology

, Volume 55, Issue 7, pp 499–507 | Cite as

Microbial radiation-resistance mechanisms

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Abstract

Organisms living in extreme environments have evolved a wide range of survival strategies by changing biochemical and physiological features depending on their biological niches. Interestingly, organisms exhibiting high radiation resistance have been discovered in the three domains of life (Bacteria, Archaea, and Eukarya), even though a naturally radiationintensive environment has not been found. To counteract the deleterious effects caused by radiation exposure, radiation- resistant organisms employ a series of defensive systems, such as changes in intracellular cation concentration, excellent DNA repair systems, and efficient enzymatic and non-enzymatic antioxidant systems. Here, we overview past and recent findings about radiation-resistance mechanisms in the three domains of life for potential usage of such radiationresistant microbes in the biotechnology industry.

Keywords

radiation DNA damage reactive oxygen species antioxidant mechanism microorganism 

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References

  1. Anderson, A.W., Nordon, H.C., Cain, R.F., Parrish, G., and Duggan, D. 1956. Studies on a radio-resistant micrococcus. I. isolation, morphology, cultural characteristics, and resistance to gamma radiation. Food Technol. 10, 576–578.Google Scholar
  2. Appukuttan, D., Singh, H., Park, S.H., Jung, J.H., Jeong, S., Seo, H.S., Choi, Y.J., and Lim, S. 2015. Engineering synthetic multistress tolerance in Escherichia coli by using a deinococcal response regulator, DR1558. Appl. Environ. Microbiol. 82, 1154–1166.PubMedCrossRefGoogle Scholar
  3. Azzam, E.I., Jay-Gerin, J.P., and Pain, D. 2012. Ionizing radiationinduced metabolic oxidative stress and prolonged cell injury. Cancer Lett. 327, 48–60.PubMedCrossRefGoogle Scholar
  4. Bagwell, C.E., Bhat, S., Hawkins, G.M., Smith, B.W., Biswas, T., Hoover, T.R., Saunders, E., Han, C.S., Tsodikov, O.V., and Shimkets, L.J. 2008a. Survival in nuclear waste, extreme resistance, and potential applications gleaned from the genome sequence of Kineococcus radiotolerans SRS30216. PLoS One 3, e3878.CrossRefGoogle Scholar
  5. Bagwell, C.E., Milliken, C.E., Ghoshroy, S., and Blom, D.A. 2008b. Intracellular copper accumulation enhances the growth of Kineococcus radiotolerans during chronic irradiation. Appl. Environ. Microbiol. 74, 1376–1384.PubMedPubMedCentralCrossRefGoogle Scholar
  6. Baliga, N.S., Bjork, S.J., Bonneau, R., Pan, M., Iloanusi, C., Kottemann, M.C., Hood, L., and DiRuggiero, J. 2004. Systems level insights into the stress response to UV radiation in the halophilic archaeon Halobacterium NRC-1. Genome Res. 14, 1025–1035.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Barnese, K., Gralla, E.B., Cabelli, D.E., and Valentine, J.S. 2008. Manganous phosphate acts as a superoxide dismutase. J. Am. Chem. Soc. 130, 4604–4606.PubMedCrossRefGoogle Scholar
  8. Bentchikou, E., Servant, P., Coste, G., and Sommer, S. 2010. A major role of the RecFOR pathway in DNA double-strand-break repair through ESDSA in Deinococcus radiodurans. PLoS Genet. 6, e1000774.CrossRefGoogle Scholar
  9. Berlett, B.S., Chock, P.B., Yim, M.B., and Stadtman, E.R. 1990. Manganese( II) catalyzes the bicarbonate-dependent oxidation of amino acids by hydrogen peroxide and the amino acid-facilitated dismutation of hydrogen peroxide. Proc. Natl. Acad. Sci. USA 87, 389–393.PubMedPubMedCentralCrossRefGoogle Scholar
  10. Breuert, S., Allers, T., Spohn, G., and Soppa, J. 2006. Regulated polyploidy in halophilic archaea. PLoS One 1, e92.CrossRefGoogle Scholar
  11. Bruce, A.K. 1964. Extraction of the radioresistant factor of Micro coccus radiodurans. Radiat. Res. 22, 155–164.PubMedCrossRefGoogle Scholar
  12. Bryan, R., Jiang, Z., Friedman, M., and Dadachova, E. 2011. The effects of gamma radiation, UV and visible light on ATP levels in yeast cells depend on cellular melanization. Fungal Biol. 115, 945–949.PubMedCrossRefGoogle Scholar
  13. Burrell, A.D., Feldschreiber, P., and Dean, C.J. 1971. DNA-membrane association and the repair of double breaks in X-irradiated Micrococcus radiodurans. Biochim. Biophys. Acta 247, 38–53.PubMedCrossRefGoogle Scholar
  14. Carreto, L., Moore, E., Nobre, M.F., Wait, R., Riley, P.W., Sharp, R.J., and da Costa, M.S. 1996. Rubrobacter xylanophilus sp. nov., a new thermophilic species isolated from a thermally polluted effluent. Int. J. Sys. Bacteriol. 46, 460–465.CrossRefGoogle Scholar
  15. Chen, Z., Li, L., Shan, Z., Huang, H., Chen, H., Ding, X., Guo, J., and Liu, L. 2016. Transcriptome sequencing analysis of novel sRNAs of Kineococcus radiotolerans in response to ionizing radiation. Microbiol. Res. 192, 122–129.PubMedCrossRefGoogle Scholar
  16. Close, D.M., Nelson, W.H., and Bernhard, W.A. 2013. DNA damage by the direct effect of ionizing radiation: products produced by two sequential one-electron oxidations. J. Phys. Chem. A 117, 12608–12615.PubMedCrossRefGoogle Scholar
  17. Confalonieri, F. and Sommer, S. 2011. Bacterial and archaeal resistance to ionizing radiation. J. Phys.: Conf. Ser. 261.Google Scholar
  18. Cox, M.M. and Battista, J.R. 2005. Deinococcus radiodurans - the consummate survivor. Nat. Rev. Microbiol. 3, 882–892.PubMedCrossRefGoogle Scholar
  19. Dadachova, E., Bryan, R.A., Howell, R.C., Schweitzer, A.D., Aisen, P., Nosanchuk, J.D., and Casadevall, A. 2008. The radioprotective properties of fungal melanin are a function of its chemical composition, stable radical presence and spatial arrangement. Pigment Cell Melanoma Res. 21, 192–199.PubMedCrossRefGoogle Scholar
  20. Dadachova, E., Bryan, R.A., Huang, X., Moadel, T., Schweitzer, A.D., Aisen, P., Nosanchuk, J.D., and Casadevall, A. 2007. Ionizing radiation changes the electronic properties of melanin and enhances the growth of melanized fungi. PLoS One 2, e457.CrossRefGoogle Scholar
  21. Dadachova, E. and Casadevall, A. 2008. Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr. Opin. Microbiol. 11, 525–531.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Dalle-Donne, I., Aldini, G., Carini, M., Colombo, R., Rossi, R., and Milzani, A. 2006. Protein carbonylation, cellular dysfunction, and disease progression. J. Cell. Mol. Med. 10, 389–406.PubMedCrossRefGoogle Scholar
  23. Daly, M.J. 2009. A new perspective on radiation resistance based on Deinococcus radiodurans. Nat. Rev. Microbiol. 7, 237–245.PubMedCrossRefGoogle Scholar
  24. Daly, M.J. 2012. Death by protein damage in irradiated cells. DNA Repair (Amst) 11, 12–21.CrossRefGoogle Scholar
  25. Daly, M.J., Gaidamakova, E.K., Matrosova, V.Y., Kiang, J.G., Fukumoto, R., Lee, D.Y., Wehr, N.B., Viteri, G.A., Berlett, B.S., and Levine, R.L. 2010. Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS One 5, e12570.CrossRefGoogle Scholar
  26. Daly, M.J., Gaidamakova, E.K., Matrosova, V.Y., Vasilenko, A., Zhai, M., Leapman, R.D., Lai, B., Ravel, B., Li, S.M., Kemner, K.M., et al. 2007. Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol. 5, e92.CrossRefGoogle Scholar
  27. Daly, M.J., Gaidamakova, E.K., Matrosova, V.Y., Vasilenko, A., Zhai, M., Venkateswaran, A., Hess, M., Omelchenko, M.V., Kostandarithes, H.M., Makarova, K.S., et al. 2004. Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306, 1025–1028.PubMedCrossRefGoogle Scholar
  28. DiRuggiero, J., Santangelo, N., Nackerdien, Z., Ravel, J., and Robb, F.T. 1997. Repair of extensive ionizing-radiation DNA damage at 95°C in the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 179, 4643–4645.PubMedPubMedCentralCrossRefGoogle Scholar
  29. Duine, J.A. 1990. PQQ, an elusive coenzyme? Trends Biochem. Sci. 15, 96–97.PubMedCrossRefGoogle Scholar
  30. Earl, A.M., Mohundro, M.M., Mian, I.S., and Battista, J.R. 2002. The IrrE protein of Deinococcus radiodurans R1 is a novel regulator of recA expression. J. Bacteriol. 184, 6216–6224.PubMedPubMedCentralCrossRefGoogle Scholar
  31. Engel, M.B. and Catchpole, H.R. 2005. A microprobe analysis of inorganic elements in Halobacterium salinarum. Cell. Biol. Int. 29, 616–622.PubMedCrossRefGoogle Scholar
  32. Ferreira, A.C., Nobre, M.F., Moore, E., Rainey, F.A., Battista, J.R., and da Costa, M.S. 1999. Characterization and radiation resistance of new isolates of Rubrobacter radiotolerans and Rubrobacter xylanophilus. Extremophiles 3, 235–238.PubMedCrossRefGoogle Scholar
  33. Gabani, P. and Singh, O.V. 2013. Radiation-resistant extremophiles and their potential in biotechnology and therapeutics. Appl. Microbiol. Biotechnol. 97, 993–1004.PubMedCrossRefGoogle Scholar
  34. Gaidamakova, E.K., Myles, I.A., McDaniel, D.P., Fowler, C.J., Valdez, P.A., Naik, S., Gayen, M., Gupta, P., Sharma, A., Glass, P.J., et al. 2012. Preserving immunogenicity of lethally irradiated viral and bacterial vaccine epitopes using a radio-protective Mn2+- eptide complex from Deinococcus. Cell Host Microbe 12, 117–124.PubMedPubMedCentralCrossRefGoogle Scholar
  35. Gasch, A.P., Huang, M., Metzner, S., Botstein, D., Elledge, S.J., and Brown, P.O. 2001. Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Mol. Biol. Cell. 12, 2987–3003.PubMedPubMedCentralCrossRefGoogle Scholar
  36. Gerard, E., Jolivet, E., Prieur, D., and Forterre, P. 2001. DNA protection mechanisms are not involved in the radioresistance of the hyperthermophilic archaea Pyrococcus abyssi and P. furiosus. Mol. Genet. Genomics 266, 72–78.PubMedCrossRefGoogle Scholar
  37. Ghosh, S., Ramirez-Peralta, A., Gaidamakova, E., Zhang, P., Li, Y.Q., Daly, M.J., and Setlow, P. 2011. Effects of Mn levels on resistance of Bacillus megaterium spores to heat, radiation and hydrogen peroxide. J. Appl. Microbiol. 111, 663–670.PubMedCrossRefGoogle Scholar
  38. Halliwell, B. and Gutteridge, J. 1999. Free Radicals in Biology and Medicine, 3rd ed. Oxford University Press, Oxford.Google Scholar
  39. Hansen, M.T. 1978. Multiplicity of genome equivalents in the radiation-resistant bacterium Micrococcus radiodurans. J. Bacteriol. 134, 71–75.PubMedPubMedCentralGoogle Scholar
  40. Hoeijmakers, J.H. 2001. Genome maintenance mechanisms for preventing cancer. Nature 411, 366–374.PubMedCrossRefGoogle Scholar
  41. Hua, Y., Narumi, I., Gao, G., Tian, B., Satoh, K., Kitayama, S., and Shen, B. 2003. PprI: a general switch responsible for extreme radioresistance of Deinococcus radiodurans. Biochem. Biophys. Res. Commun. 306, 354–360.PubMedCrossRefGoogle Scholar
  42. Idnurm, A., Bahn, Y.S., Nielsen, K., Lin, X., Fraser, J.A., and Heitman, J. 2005. Deciphering the model pathogenic fungus Cryptococcus neoformans. Nat. Rev. Microbiol. 3, 753–764.PubMedCrossRefGoogle Scholar
  43. Jolivet, E., L’Haridon, S., Corre, E., Forterre, P., and Prieur, D. 2003a. Thermococcus gammatolerans sp. nov., a hyperthermophilic archaeon from a deep-sea hydrothermal vent that resists ionizing radiation. Int. J. Syst. Evol. Microbiol. 53, 847–851.PubMedCrossRefGoogle Scholar
  44. Jolivet, E., Matsunaga, F., Ishino, Y., Forterre, P., Prieur, D., and Myllykallio, H. 2003b. Physiological responses of the hyperthermophilic archaeon “Pyrococcus abyssi” to DNA damage caused by ionizing radiation. J. Bacteriol. 185, 3958–3961.PubMedPubMedCentralCrossRefGoogle Scholar
  45. Jung, K.W., Yang, D.H., Kim, M.K., Seo, H.S., Lim, S., and Bahn, Y.S. 2016. Unraveling fungal radiation resistance regulatory networks through the genome-wide transcriptome and genetic analyses of Cryptococcus neoformans. mBio 7, e01483–16.CrossRefGoogle Scholar
  46. Karam, P.A. and Leslie, S.A. 1999. Calculations of background betagamma radiation dose through geologic time. Health Phys. 77, 662–667.PubMedCrossRefGoogle Scholar
  47. Khairnar, N.P., Misra, H.S., and Apte, S.K. 2003. Pyrroloquinolinequinone synthesized in Escherichia coli by pyrroloquinolinequinone synthase of Deinococcus radiodurans plays a role beyond mineral phosphate solubilization. Biochem. Biophys. Res. Commun. 312, 303–308.PubMedCrossRefGoogle Scholar
  48. Khajo, A., Bryan, R.A., Friedman, M., Burger, R.M., Levitsky, Y., Casadevall, A., Magliozzo, R.S., and Dadachova, E. 2011. Protection of melanized Cryptococcus neoformans from lethal dose gamma irradiation involves changes in melanin’s chemical structure and paramagnetism. PLoS One 6, e25092.CrossRefGoogle Scholar
  49. Kimura, N. and Tsuge, T. 1993. Gene cluster involved in melanin biosynthesis of the filamentous fungus Alternaria alternata. J. Bacteriol. 175, 4427–4435.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Kish, A. and DiRuggiero, J. 2008. Rad50 is not essential for the Mre11-dependent repair of DNA double-strand breaks in Halobacterium sp. strain NRC-1. J. Bacteriol. 190, 5210–5216.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kish, A., Kirkali, G., Robinson, C., Rosenblatt, R., Jaruga, P., Dizdaroglu, M., and DiRuggiero, J. 2009. Salt shield: intracellular salts provide cellular protection against ionizing radiation in the halophilic archaeon, Halobacterium salinarum NRC-1. Environ. Microbiol. 11, 1066–1078.PubMedCrossRefGoogle Scholar
  52. Kitayama, S. and Matsuyama, A. 1971. Mechanism for radiation lethality in M. radiodurans. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 19, 13–19.PubMedCrossRefGoogle Scholar
  53. Kokoeva, M.V., Storch, K.F., Klein, C., and Oesterhelt, D. 2002. A novel mode of sensory transduction in archaea: binding proteinmediated chemotaxis towards osmoprotectants and amino acids. EMBO J. 21, 2312–2322.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Kottemann, M., Kish, A., Iloanusi, C., Bjork, S., and DiRuggiero, J. 2005. Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC1 to desiccation and gamma irradiation. Extremophiles 9, 219–227.PubMedCrossRefGoogle Scholar
  55. Krasin, F. and Hutchinson, F. 1977. Repair of DNA double-strand breaks in Escherichia coli, which requires recA function and the presence of a duplicate genome. J. Mol. Biol. 116, 81–98.PubMedCrossRefGoogle Scholar
  56. Kwon-Chung, K.J., Polacheck, I., and Popkin, T.J. 1982. Melaninlacking mutants of Cryptococcus neoformans and their virulence for mice. J. Bacteriol. 150, 1414–1421.PubMedPubMedCentralGoogle Scholar
  57. Li, L., Chen, Z., Ding, X., Shan, Z., Liu, L., and Guo, J. 2015. Deep sequencing analysis of the Kineococcus radiotolerans transcriptome in response to ionizing radiation. Microbiol. Res. 170, 248–254.PubMedCrossRefGoogle Scholar
  58. Lin, J., Qi, R., Aston, C., Jing, J., Anantharaman, T.S., Mishra, B., White, O., Daly, M.J., Minton, K.W., Venter, J.C., et al. 1999. Whole-genome shotgun optical mapping of Deinococcus radiodurans. Science 285, 1558–1562.PubMedCrossRefGoogle Scholar
  59. Liu, Y., Zhou, J., Omelchenko, M.V., Beliaev, A.S., Venkateswaran, A., Stair, J., Wu, L., Thompson, D.K., Xu, D., Rogozin, I.B., et al. 2003. Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc. Natl. Acad. Sci. USA 100, 4191–4196.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Lu, H., Gao, G., Xu, G., Fan, L., Yin, L., Shen, B., and Hua, Y. 2009. Deinococcus radiodurans PprI switches on DNA damage response and cellular survival networks after radiation damage. Mol. Cell. Proteomics 8, 481–494.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Madian, A.G. and Regnier, F.E. 2010. Proteomic identification of carbonylated proteins and their oxidation sites. J. Proteome Res. 9, 3766–3780.PubMedPubMedCentralCrossRefGoogle Scholar
  62. Maisonneuve, E., Ducret, A., Khoueiry, P., Lignon, S., Longhi, S., Talla, E., and Dukan, S. 2009. Rules governing selective protein carbonylation. PLoS One 4, e7269.CrossRefGoogle Scholar
  63. Makarova, K.S., Aravind, L., Wolf, Y.I., Tatusov, R.L., Minton, K.W., Koonin, E.V., and Daly, M.J. 2001. Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol. Mol. Biol. Rev. 65, 44–79.PubMedPubMedCentralCrossRefGoogle Scholar
  64. Makarova, K.S., Omelchenko, M.V., Gaidamakova, E.K., Matrosova, V.Y., Vasilenko, A., Zhai, M., Lapidus, A., Copeland, A., Kim, E., Land, M., et al. 2007. Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks. PLoS One 2, e955.CrossRefGoogle Scholar
  65. Marguet, E. and Forterre, P. 1998. Protection of DNA by salts against thermodegradation at temperatures typical for hyperthermophiles. Extremophiles 2, 115–122.PubMedCrossRefGoogle Scholar
  66. Markillie, L.M., Varnum, S.M., Hradecky, P., and Wong, K.K. 1999. Targeted mutagenesis by duplication insertion in the radioresistant bacterium Deinococcus radiodurans: radiation sensitivities of catalase (katA) and superoxide dismutase (sodA) mutants. J. Bacteriol. 181, 666–669.PubMedPubMedCentralGoogle Scholar
  67. McNaughton, R.L., Reddi, A.R., Clement, M.H., Sharma, A., Barnese, K., Rosenfeld, L., Gralla, E.B., Valentine, J.S., Culotta, V.C., and Hoffman, B.M. 2010. Probing in vivo Mn2+ speciation and oxidative stress resistance in yeast cells with electron-nuclear double resonance spectroscopy. Proc. Natl. Acad. Sci. USA 107, 15335–15339.PubMedPubMedCentralCrossRefGoogle Scholar
  68. Mironenko, N.V., Alekhina, I.A., Zhdanova, N.N., and Bulat, S.A. 2000. Intraspecific variation in gamma-radiation resistance and genomic structure in the filamentous fungus Alternaria alternata: a case study of strains inhabiting Chernobyl reactor no. 4. Ecotoxicol. Environ. Saf. 45, 177–187.PubMedCrossRefGoogle Scholar
  69. Misra, H.S., Khairnar, N.P., Barik, A., Indira Priyadarsini, K., Mohan, H., and Apte, S.K. 2004. Pyrroloquinoline-quinone: a reactive oxygen species scavenger in bacteria. FEBS Lett. 578, 26–30.PubMedCrossRefGoogle Scholar
  70. Narumi, I., Satoh, K., Cui, S., Funayama, T., Kitayama, S., and Watanabe, H. 2004. PprA: a novel protein from Deinococcus radiodurans that stimulates DNA ligation. Mol. Microbiol. 54, 278–285.PubMedCrossRefGoogle Scholar
  71. Norais, C.A., Chitteni-Pattu, S., Wood, E.A., Inman, R.B., and Cox, M.M. 2009. DdrB protein, an alternative Deinococcus radiodurans SSB induced by ionizing radiation. J. Biol. Chem. 284, 21402–21411.PubMedPubMedCentralCrossRefGoogle Scholar
  72. Nosanchuk, J.D. and Casadevall, A. 2003. The contribution of melanin to microbial pathogenesis. Cell. Microbiol. 5, 203–223.PubMedCrossRefGoogle Scholar
  73. Pacelli, C., Bryan, R.A., Onofri, S., Selbmann, L., Shuryak, I., and Dadachova, E. 2017. Melanin is effective in protecting fast and slow growing fungi from various types of ionizing radiation. Environ. Microbiol. 19, 1612–1624.PubMedCrossRefGoogle Scholar
  74. Park, S.H., Singh, H., Appukuttan, D., Jeong, S., Choi, Y.J., Jung, J.H., Narumi, I., and Lim, S. 2016. PprM, a cold shock domaincontaining protein from Deinococcus radiodurans, confers oxidative stress tolerance to Escherichia coli. Front. Microbiol. 7, 2124.PubMedGoogle Scholar
  75. Phillips, R.W., Wiegel, J., Berry, C.J., Fliermans, C., Peacock, A.D., White, D.C., and Shimkets, L.J. 2002. Kineococcus radiotolerans sp. nov., a radiation-resistant, gram-positive bacterium. Int. J. Sys. Evol. Microbiol. 52, 933–938.Google Scholar
  76. Rainey, F.A., Ray, K., Ferreira, M., Gatz, B.Z., Nobre, M.F., Bagaley, D., Rash, B.A., Park, M.J., Earl, A.M., Shank, N.C., et al. 2005. Extensive diversity of ionizing-radiation-resistant bacteria recovered from Sonoran Desert soil and description of nine new species of the genus Deinococcus obtained from a single soil sample. Appl. Environ. Microbiol. 71, 5225–5235.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Rajpurohit, Y.S., Gopalakrishnan, R., and Misra, H.S. 2008. Involvement of a protein kinase activity inducer in DNA double strand break repair and radioresistance of Deinococcus radiodurans. J. Bacteriol. 190, 3948–3954.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Repar, J., Cvjetan, S., Slade, D., Radman, M., Zahradka, D., and Zahradka, K. 2010. RecA protein assures fidelity of DNA repair and genome stability in Deinococcus radiodurans. DNA Repair (Amst) 9, 1151–1161.CrossRefGoogle Scholar
  79. Rich, T., Allen, R.L., and Wyllie, A.H. 2000. Defying death after DNA damage. Nature 407, 777–783.PubMedCrossRefGoogle Scholar
  80. Robinson, C.K., Webb, K., Kaur, A., Jaruga, P., Dizdaroglu, M., Baliga, N.S., Place, A., and Diruggiero, J. 2011. A major role for nonenzymatic antioxidant processes in the radioresistance of Halobacterium salinarum. J. Bacteriol. 193, 1653–1662.PubMedPubMedCentralCrossRefGoogle Scholar
  81. Saito, T., Miyabe, Y., Ide, H., and Yamanoto, O. 1997. Hydroxyl radical scavenging ability of bacterioruberin. Raddiat. Phys. Chem. 50, 267–269.CrossRefGoogle Scholar
  82. Saito, T., Terato, H., and Yamamoto, O. 1994. Pigments of Rubrobacter radiotolerans. Arch. Microbiol. 162, 414–421.CrossRefGoogle Scholar
  83. Saleh, Y.G., Mayo, M.S., and Ahearn, D.G. 1988. Resistance of some common fungi to gamma irradiation. Appl. Environ. Microbiol. 54, 2134–2135.PubMedPubMedCentralGoogle Scholar
  84. Sghaier, H., Ghedira, K., Benkahla, A., and Barkallah, I. 2008. Basal DNA repair machinery is subject to positive selection in ionizing-radiation-resistant bacteria. BMC Genomics 9, 297.PubMedPubMedCentralCrossRefGoogle Scholar
  85. Shahmohammadi, H.R., Asgarani, E., Terato, H., Saito, T., Ohyama, Y., Gekko, K., Yamamoto, O., and Ide, H. 1998. Protective roles of bacterioruberin and intracellular KCl in the resistance of Halobacterium salinarium against DNA-damaging agents. J. Radiat. Res. 39, 251–262.PubMedCrossRefGoogle Scholar
  86. Slade, D. and Radman, M. 2011. Oxidative stress resistance in Deinococcus radiodurans. Microbiol. Mol. Biol. Rev. 75, 133–191.PubMedPubMedCentralCrossRefGoogle Scholar
  87. Stahl, W. and Sies, H. 2003. Antioxidant activity of carotenoids. Mol. Aspects Med. 24, 345–351.PubMedCrossRefGoogle Scholar
  88. Stan-Lotter, H. and Fendrihan, S. 2012. Adaptation of microbial life to environmental extremesCrossRefGoogle Scholar
  89. Sukharev, S.A., Pleshakova, O.V., Moshnikova, A.B., Sadovnikov, V.B., and Gaziev, A.I. 1997. Age-and radiation-dependent changes in carbonyl content, susceptibility to proteolysis, and antigenicity of soluble rat liver proteins. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 116, 333–338.PubMedCrossRefGoogle Scholar
  90. Suzuki, K., Collins, M.D., Iijima, E., and Komagata, K. 1988. Chemotaxonomic characterization of a radiotolerant bacterium, Arthrobacter radiotolerans: Description of Rubrobacter radiotolerans gen. nov., comb. nov. FEMS Microbiol. Lett. 52, 33–39.CrossRefGoogle Scholar
  91. Tanaka, M., Earl, A.M., Howell, H.A., Park, M.J., Eisen, J.A., Peterson, S.N., and Battista, J.R. 2004. Analysis of Deinococcus radiodurans’s transcriptional response to ionizing radiation and desiccation reveals novel proteins that contribute to extreme radioresistance. Genetics 168, 21–33.PubMedPubMedCentralCrossRefGoogle Scholar
  92. Tapias, A., Leplat, C., and Confalonieri, F. 2009. Recovery of ionizing-radiation damage after high doses of gamma ray in the hyperthermophilic archaeon Thermococcus gammatolerans. Extremophiles 13, 333–343.PubMedCrossRefGoogle Scholar
  93. Tatsuzawa, H., Maruyama, T., Misawa, N., Fujimori, K., and Nakano, M. 2000. Quenching of singlet oxygen by carotenoids produced in Escherichia coli - attenuation of singlet oxygen-mediated bacterial killing by carotenoids. FEBS Lett. 484, 280–284.PubMedCrossRefGoogle Scholar
  94. Terato, H., Kobayashi, M., Yamamoto, O., and Ide, H. 1999. DNA strand breaks induced by ionizing radiation on Rubrobacter radiotolerans, an extremely radioresistant bacterium. Microbiol. Res. 154, 173–178.CrossRefGoogle Scholar
  95. Tian, B., Wu, Y., Sheng, D., Zheng, Z., Gao, G., and Hua, Y. 2004. Chemiluminescence assay for reactive oxygen species scavenging activities and inhibition on oxidative damage of DNA in Deinococcus radiodurans. Luminescence 19, 78–84.PubMedCrossRefGoogle Scholar
  96. Tian, B., Xu, Z., Sun, Z., Lin, J., and Hua, Y. 2007. Evaluation of the antioxidant effects of carotenoids from Deinococcus radiodurans through targeted mutagenesis, chemiluminescence, and DNA damage analyses. Biochim. Biophys. Acta 1770, 902–911.PubMedCrossRefGoogle Scholar
  97. Vember, V.V. and Zhdanova, N.N. 2001. Peculiarities of linear growth of the melanin-containing fungi Cladosporium sphaerospermum Penz. and Alternaria alternata (Fr.) Keissler. Mikrobiol. Z. 63, 3–12.PubMedGoogle Scholar
  98. Watson, A., Mata, J., Bahler, J., Carr, A., and Humphrey, T. 2004. Global gene expression responses of fission yeast to ionizing radiation. Mol. Biol. Cell 15, 851–860.PubMedPubMedCentralCrossRefGoogle Scholar
  99. Webb, K.M. and DiRuggiero, J. 2012. Role of Mn2+ and compatible solutes in the radiation resistance of thermophilic bacteria and archaea. Archaea 2012, 845756.PubMedPubMedCentralCrossRefGoogle Scholar
  100. Webb, K.M., Yu, J., Robinson, C.K., Noboru, T., Lee, Y.C., and DiRuggiero, J. 2013. Effects of intracellular Mn on the radiation resistance of the halophilic archaeon Halobacterium salinarum. Extremophiles 17, 485–497.PubMedCrossRefGoogle Scholar
  101. White, O., Eisen, J.A., Heidelberg, J.F., Hickey, E.K., Peterson, J.D., Dodson, R.J., Haft, D.H., Gwinn, M.L., Nelson, W.C., Richardson, D.L., et al. 1999. Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286, 1571–1577.PubMedPubMedCentralCrossRefGoogle Scholar
  102. Whitehead, K., Kish, A., Pan, M., Kaur, A., Reiss, D.J., King, N., Hohmann, L., DiRuggiero, J., and Baliga, N.S. 2006. An integrated systems approach for understanding cellular responses to gamma radiation. Mol. Syst. Biol. 2, 47.PubMedPubMedCentralCrossRefGoogle Scholar
  103. Williams, E., Lowe, T.M., Savas, J., and DiRuggiero, J. 2007. Microarray analysis of the hyperthermophilic archaeon Pyrococcus furiosus exposed to gamma irradiation. Extremophiles 11, 19–29.PubMedCrossRefGoogle Scholar
  104. Williamson, P.R. 1994. Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. J. Bacteriol. 176, 656–664.PubMedPubMedCentralCrossRefGoogle Scholar
  105. Xu, Z., Tian, B., Sun, Z., Lin, J., and Hua, Y. 2007. Identification and functional analysis of a phytoene desaturase gene from the extremely radioresistant bacterium Deinococcus radiodurans. Microbiology 153, 1642–1652.PubMedCrossRefGoogle Scholar
  106. Yoshinaka, T., Yano, K., and Yamaguchi, H. 1973. Isolation of highly radioresistant bacterium Arthrobacter radiotolerans nov. sp. Agr. Bioi. Chem. 37, 2269–2275.CrossRefGoogle Scholar
  107. Zahradka, K., Slade, D., Bailone, A., Sommer, S., Averbeck, D., Petranovic, M., Lindner, A.B., and Radman, M. 2006. Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature 443, 569–573.PubMedGoogle Scholar
  108. Zhang, L., Yang, Q., Luo, X., Fang, C., Zhang, Q., and Tang, Y. 2007. Knockout of crtB or crtI gene blocks the carotenoid biosynthetic pathway in Deinococcus radiodurans R1 and influences its resistance to oxidative DNA-damaging agents due to change of free radicals scavenging ability. Arch. Microbiol. 188, 411–419.PubMedCrossRefGoogle Scholar
  109. Zhdanova, N.N., Lashko, T.N., Redchits, T.I., Vasilevskaia, A.I., Borisiuk, L.G., Siniavskaia, O.I., Gavriliuk, V.I., and Muzalev, P.N. 1991. The interaction of soil micromycetes with “hot” particles in a model system. Mikrobiol. Z. 53, 9–17.Google Scholar
  110. Zhdanova, N.N., Tugay, T., Dighton, J., Zheltonozhsky, V., and Mc-Dermott, P. 2004. Ionizing radiation attracts soil fungi. Mycol. Res. 108, 1089–1096.PubMedCrossRefGoogle Scholar
  111. Zivanovic, Y., Armengaud, J., Lagorce, A., Leplat, C., Guerin, P., Dutertre, M., Anthouard, V., Forterre, P., Wincker, P., and Confalonieri, F. 2009. Genome analysis and genome-wide proteomics of Thermococcus gammatolerans, the most radioresistant organism known amongst the Archaea. Genome Biol. 10, R70.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Research Division for BiotechnologyKorea Atomic Energy Research InstituteJeongeupRepublic of Korea
  2. 2.Department of BiotechnologyCollege of Life Science and Biotechnology, Yonsei UniversitySeoulRepublic of Korea

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