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A new perspective on radiation resistance based on Deinococcus radiodurans

Nature Reviews Microbiology volume 7, pages 237–245 (2009)Cite this article

Abstract

In classical models of radiation toxicity, DNA is the molecule that is most affected by ionizing radiation (IR). However, recent data show that the amount of protein damage caused during irradiation of bacteria is better related to survival than to DNA damage. In this Opinion article, a new model is presented in which proteins are the most important target in the hierarchy of macromolecules affected by IR. A first line of defence against IR in extremely radiation-resistant bacteria might be the accumulation of manganese complexes, which can prevent the production of iron-dependent reactive oxygen species. This would allow an irradiated cell to protect sufficient enzymatic activity needed to repair DNA and survive.

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Figure 1: Relationship between survival following exposure to ionizing radiation and intracellular manganese and iron contents.
Figure 2: In vivo ionizing radiation-induced oxidative protein damage.
Figure 3: Model of ionizing radiation-driven manganese and iron redox cycling.
Figure 4: X-ray fluorescence maps of the qualitative distribution and concentration gradients of various metals and non-metals in Deinococcus radiodurans.

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References

  1. Thornley, M. J. Radiation resistance among bacteria. J. Appl. Bacteriol. 26, 334–345 (1963).

    Article  Google Scholar 

  2. Parashar, V., Frankel, S., Lurie, A. G. & Rogina, B. The effects of age on radiation resistance and oxidative stress in adult Drosophila melanogaster. Radiat. Res. 169, 707–711 (2008).

    Article  CAS  PubMed  Google Scholar 

  3. Gladyshev, E. & Meselson, M. Extreme resistance of bdelloid rotifers to ionizing radiation. Proc. Natl Acad. Sci. USA 105, 5139–5144 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Horikawa, D. D. et al. Radiation tolerance in the tardigrade Milnesium tardigradum. Int. J. Radiat. Biol. 82, 843–848 (2006).

    Article  CAS  PubMed  Google Scholar 

  5. Johnson, T. E. & Hartman, P. S. Radiation effects on life span in Caenorhabditis elegans. J. Gerontol. 43, B137–B141 (1988).

    Article  CAS  PubMed  Google Scholar 

  6. Holloman, W. K., Schirawski, J. & Holliday, R. Towards understanding the extreme radiation resistance of Ustilago maydis. Trends Microbiol. 15, 525–529 (2007).

    Article  CAS  PubMed  Google Scholar 

  7. DiRuggiero, J., Santangelo, N., Nackerdien, Z., Ravel, J. & Robb, F. T. Repair of extensive ionizing-radiation DNA damage at 95°C in the hyperthermophilic archaeon Pyrococcus furiosus. J. Bacteriol. 179, 4643–4645 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kottemann, M., Kish, A., Iloanusi, C., Bjork, S. & DiRuggiero, J. Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC1 to desiccation and gamma irradiation. Extremophiles 9, 219–227 (2005).

    Article  CAS  PubMed  Google Scholar 

  9. Daly, M. J., Ouyang, L., Fuchs, P. & Minton, K. W. In vivo damage and recA-dependent repair of plasmid and chromosomal DNA in the radiation-resistant bacterium Deinococcus radiodurans. J. Bacteriol. 176, 3508–3517 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Hutchinson, F. The molecular basis for radiation effects on cells. Cancer Res. 26, 2045–2052 (1966).

    CAS  PubMed  Google Scholar 

  11. von Sonntag, C. The Chemical Basis of Radiation Biology (Taylor & Francis, London, 1987).

    Google Scholar 

  12. Daly, M. J. & Minton, K. W. Interchromosomal recombination in the extremely radioresistant bacterium Deinococcus radiodurans. J. Bacteriol. 177, 5495–5505 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Holliday, R. Early studies on recombination and DNA repair in Ustilago maydis. DNA Repair 3, 671–682 (2004).

    Article  CAS  PubMed  Google Scholar 

  14. Cox, M. M. & Battista, J. R. Deinococcus radiodurans — the consummate survivor. Nature Rev. Microbiol. 3, 882–892 (2005).

    Article  CAS  Google Scholar 

  15. Daly, M. J. & Minton, K. W. An alternative pathway of recombination of chromosomal fragments precedes recA-dependent recombination in the radioresistant bacterium Deinococcus radiodurans. J. Bacteriol. 178, 4461–4471 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Daly, M. J. et al. Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306, 1025–1028 (2004).

    Article  CAS  PubMed  Google Scholar 

  17. Gerard, E., Jolivet, E., Prieur, D. & Forterre, P. DNA protection mechanisms are not involved in the radioresistance of the hyperthermophilic archaea Pyrococcus abyssi and P. furiosus. Mol. Genet. Genomics 266, 72–78 (2001).

    Article  CAS  PubMed  Google Scholar 

  18. Argueso, J. L. et al. Double-strand breaks associated with repetitive DNA can reshape the genome. Proc. Natl Acad. Sci. USA 105, 11845–11850 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Setlow, D. M. & Duggan, D. E. The resistance of Micrococcus radiodurans to ultraviolet radiation: ultraviolet-induced lesions in the cell's DNA. Biochim.Biophys. Acta 87, 664–668 (1964).

    CAS  PubMed  Google Scholar 

  20. Kish, A. et al. Salt shield: intracellular salts provide cellular protection against ionizing radiation in the halophilic archaeon, Halobacterium salinarum NRC-1. Environ. Microbiol. 5 Jan 2009 (doi:10.1111/j.1462-2920.2008.01828.x).

    Article  CAS  PubMed  Google Scholar 

  21. Chan, H. L. et al. Proteomic analysis of UVC irradiation-induced damage of plasma proteins: serum amyloid P component as a major target of photolysis. FEBS Lett. 580, 3229–3236 (2006).

    Article  CAS  PubMed  Google Scholar 

  22. Ghosal, D. et al. How radiation kills cells: survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress. FEMS Microbiol. Rev. 29, 361–375 (2005).

    CAS  PubMed  Google Scholar 

  23. Makarova, K. S. et al. Genome of the extremely radiation resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol. Mol. Biol. Rev. 65, 44–79 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Daly, M. J. & Minton, K. W. Recombination between a resident plasmid and the chromosome following irradiation of the radioresistant bacterium Deinococcus radiodurans. Gene 187, 225–229 (1997).

    Article  CAS  PubMed  Google Scholar 

  25. Liu, Y. et al. Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc. Natl Acad. Sci. USA 100, 4191–4196 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Makarova, K. S. et al. Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks. PLoS ONE 9, e955 (2007).

    Article  CAS  Google Scholar 

  27. Daly, M. J. & Minton, K. W. Resistance to radiation. Science 270, 1318 (1995).

    Article  CAS  PubMed  Google Scholar 

  28. Eltsov, M. & Dubochet, J. Fine structure of the Deinococcus radiodurans nucleoid revealed by cryoelectron microscopy of vitreous sections. J. Bacteriol. 187, 8047–8054 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Dimitrova, N., Chen, Y. C., Spector, D. L. & de Lange, T. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456, 524–528 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Gutman, P. D., Fuchs, P. & Minton, K. W. Restoration of the DNA damage resistance of Deinococcus radiodurans DNA polymerase mutants by Escherichia coli DNA polymerase I and Klenow fragment. Mutat. Res. 314, 87–97 (1994).

    Article  CAS  PubMed  Google Scholar 

  31. Minton, K. W. DNA repair in the extremely radioresistant bacterium Deinococcus radiodurans. Mol. Microbiol. 13, 9–15 (1994).

    Article  CAS  PubMed  Google Scholar 

  32. Fredrickson, J. K. et al. Protein oxidation: key to bacterial desiccation resistance? ISME J. 2, 393–403 (2008).

    Article  CAS  PubMed  Google Scholar 

  33. Zahradka, K. et al. Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature 443, 569–573 (2006).

    Article  CAS  PubMed  Google Scholar 

  34. Daly, M. J. et al. Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol. 5, e92 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. White, O. et al. Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286, 1571–1577 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Gioia, J. et al. Paradoxical DNA repair and peroxide resistance gene conservation in Bacillus pumilus SAFR-032. PLoS ONE 2, e928 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Cohen, G. N. et al. An integrated analysis of the genome of the hyperthermophilic archaeon Pyrococcus abyssi. Mol. Microbiol. 47, 1495–1512 (2003).

    Article  CAS  PubMed  Google Scholar 

  38. Ng, W. V. et al. Genome sequence of Halobacterium species NRC-1. Proc. Natl Acad. Sci. USA 97, 12176–12181 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Koonin, E. V. Chance and necessity in cellular response to challenge. Mol. Syst. Biol. 3, 107 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Harris, D. R., Ngo, K. V. & Cox, M. M. The stable, functional core of DdrA from Deinococcus radiodurans R1 does not restore radioresistance in vivo. J. Bacteriol. 190, 6475–6482 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Qiu, X. et al. Transcriptome analysis applied to survival of Shewanella oneidensis MR-1 exposed to ionizing radiation. J. Bacteriol. 188, 1199–1204 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Sweet, D. M. & Moseley, B. E. The resistance of Micrococcus radiodurans to killing and mutation by agents which damage DNA. Mutat. Res. 34, 175–186 (1976).

    Article  CAS  PubMed  Google Scholar 

  43. Sommers, C. H. & Rajkowski, K. T. Inactivation of Escherichia coli JM109, DH5α, and 0157:H7 suspended in Butterfield's phosphate buffer by gamma radiation. J. Food Sci. 73, M87–M90 (2008).

    Article  CAS  PubMed  Google Scholar 

  44. Dadachova, E. & Casadevall, A. Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. Curr. Opin. Microbiol. 11, 525–531 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Shirkey, B. et al. Genomic DNA of Nostoc commune (Cyanobacteria) becomes covalently modified during long-term (decades) desiccation but is protected from oxidative damage and degradation. Nucleic Acids Res. 31, 2995–3005 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Leibowitz, P. J., Schwartzberg, L. S. & Bruce, A. K. The in vivo association of manganese with the chromosome of Micrococcus radiodurans. Photochem. Photobiol. 23, 45–50 (1976).

    Article  CAS  PubMed  Google Scholar 

  47. Hastings, J. W., Holzapfel, W. H. & Niemand, J. G. Radiation resistance of lactobacilli isolated from radurized meat relative to growth and environment. Appl. Environ. Microbiol. 52, 898–901 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Domain, F., Houot, L., Chauvat, F. & Cassier-Chauvat, C. Function and regulation of the cyanobacterial genes lexA, recA and ruvB: LexA is critical to the survival of cells facing inorganic carbon starvation. Mol. Microbiol. 53, 65–80 (2004).

    Article  CAS  PubMed  Google Scholar 

  49. Archibald, F. S. & Fridovich, I. The scavenging of superoxide radical by manganous complexes: in vitro. Arch. Biochem. Biophys. 214, 452–463 (1982).

    Article  CAS  PubMed  Google Scholar 

  50. Keren, N., Kidd, M. J., Penner-Hahn, J. E. & Pakrasi, H. B. A light-dependent mechanism for massive accumulation of manganese in the photosynthetic bacterium Synechocystis sp. PCC 6803. Biochemistry 41, 15085–15092 (2002).

    Article  CAS  PubMed  Google Scholar 

  51. Kehres, D. G. & Maguire, M. E. Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria. FEMS Microbiol. Rev. 27, 263–290 (2003).

    Article  CAS  PubMed  Google Scholar 

  52. Sanchez, R. J. et al. Exogenous manganous ion at millimolar levels rescues all known dioxygen-sensitive phenotypes of yeast lacking CuZnSOD. J. Biol. Inorg. Chem. 10, 913–923 (2005).

    Article  CAS  PubMed  Google Scholar 

  53. Jakubovics, N. S. & Jenkinson, H. F. Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria. Microbiology 147, 1709–1718 (2001).

    Article  CAS  PubMed  Google Scholar 

  54. Lin, Y. T. et al. Manganous ion supplementation accelerates wild type development, enhances stress resistance, and rescues the life span of a short-lived Caenorhabditis elegans mutant. Free Radic. Biol. Med. 40, 1185–1193 (2006).

    Article  CAS  PubMed  Google Scholar 

  55. Puskin, J. S. & Gunter, T. E. Ion and pH gradients across the transport membrane of mitochondria following Mn(II) uptake in the presence of acetate. Biochem. Biophys. Res. Commun. 51, 797–803 (1973).

    Article  CAS  PubMed  Google Scholar 

  56. Oweson, C., Sköld, H., Pinsino, A., Matranga, V. & Hernroth, B. Manganese effects on haematopoietic cells and circulating coelomocytes of Asterias rubens (Linnaeus). Aquat. Toxicol. 89, 75–81 (2008).

    Article  CAS  PubMed  Google Scholar 

  57. Imlay, J. A. Iron–sulphur clusters and the problem with oxygen. Mol. Microbiol. 59, 1073–1082 (2006).

    Article  PubMed  Google Scholar 

  58. Barnese, K., Gralla, E. B., Cabelli, D. E. & Valentine. J. S. Manganous phosphate acts as a superoxide dismutase. J. Am. Chem. Soc. 130, 4604–4606 (2008).

    Article  CAS  PubMed  Google Scholar 

  59. Berlett, B. S., Chock, P. B., Yim, M. B. & Stadtman, E. R. 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 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Archibald, F. S. & Fridovich, I. Manganese, superoxide dismutase, and oxygen tolerance in some lactic acid bacteria. J. Bacteriol. 146, 928–936 (1981).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Imlay, J. A. Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 77, 755–776 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Marshall, M. J. et al. c-Type cytochrome-dependent formation of U(IV) nanoparticles by Shewanella oneidensis. PLoS Biol. 4, e268 (2006).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Levine R. L. & Stadtman E. R. Oxidative modification of proteins during aging. Exp. Gerontol. 36, 1495–1502 (2001).

    Article  CAS  PubMed  Google Scholar 

  64. Winter, J., Ilbert, M., Graf, P. C., Ozcelik, D. & Jakob, U. Bleach activates a redox-regulated chaperone by oxidative protein unfolding. Cell 135, 691–701 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Reyes-Lamothe, R., Wang, W. & Sherratt, D. Escherichia coli and its chromosome. Trends Microbiol. 16, 238–245 (2008).

    Article  CAS  PubMed  Google Scholar 

  66. Maeshima, K. & Eltsov, M. Packaging the genome: the structure of mitotic chromosomes. J. Biochem. 143, 145–153 (2008).

    Article  CAS  PubMed  Google Scholar 

  67. Cuypers, M. G., Mitchell, E. P., Romão, C. V. & McSweeney, S. M. The crystal structure of the Dps2 from Deinococcus radiodurans reveals an unusual pore profile with a non-specific metal binding site. J. Mol. Biol. 371, 787–799 (2007).

    Article  CAS  PubMed  Google Scholar 

  68. Serianni, R. W. & Bruce, A. K. Role of sulphur in radioprotective extracts of Micrococcus radiodurans. Nature 218, 485–487 (1968).

    Article  CAS  PubMed  Google Scholar 

  69. Lin, L.-H. et al. The yield and isotopic composition of radiolytic H2, a potential energy source for the deep subsurface biosphere. Geochim. Cosmochim. Acta 69, 893–903 (2005).

    Article  CAS  Google Scholar 

  70. Rainey, F. A. et al. 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 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Blasius, M., Sommer, S. & Hubscher, U. Deinococcus radiodurans: what belongs to the survival kit? Crit. Rev. Biochem. Mol. Biol. 43, 221–238 (2008).

    Article  CAS  PubMed  Google Scholar 

  72. Anderson, A., Nordan, H., Cain, R., Parrish, G. & Duggan, D. Studies on a radioresistant micrococcus. I. Isolation, morphology, cultural characteristics, and resistance to gamma radiation. Food Technol. 10, 575–578 (1956).

    Google Scholar 

  73. Fredrickson, J. K. et al. Geomicrobiology of high level nuclear waste contaminated vadose sediments at the Hanford Site, Washington State. Appl. Environ. Microbiol. 70, 4230–4241 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Callegan, R. P. et al. Description of four novel psychrophilic, ionizing radiation-sensitive Deinococcus species from alpine environments. Int. J. Syst. Evol. Microbiol. 58, 1252–1258 (2008).

    Article  CAS  PubMed  Google Scholar 

  75. Hirsch, P. et al. Deinococcus frigens sp. nov., Deinococcus saxicola sp. nov., and Deinococcus marmoris sp. nov., low temperature and draught-tolerating, UV-resistant bacteria from continental Antarctica. Syst. Appl. Microbiol. 27, 636–645 (2004).

    Article  CAS  PubMed  Google Scholar 

  76. Ferreira, A. C. et al. Deinococcus geothermalis sp. nov. and Deinococcus murrayi sp. nov., two extremely radiation resistant and slightly thermophilic species from hot springs. Int. J. Syst. Bacteriol. 47, 939–947 (1997).

    Article  CAS  PubMed  Google Scholar 

  77. Kimura, H., Asada, R., Masta, A. & Naganuma, T. Distribution of microorganisms in the subsurface of the manus basin hydrothermal vent field in Papua New Guinea. Appl. Environ. Microbiol. 69, 644–648 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Pavlov, A. K., Kalinin, V. L., Konstantinov, A. N., Shelegedin, V. N. & Pavlov, A. A. Was earth ever infected by martian biota? Clues from radioresistant bacteria. Astrobiology 6, 911–918 (2006).

    Article  CAS  PubMed  Google Scholar 

  79. Brim, H., Venkateswaran, A., Kostandarithes, H. M., Fredrickson, J. K. & Daly, M. J. Genetic development of D. geothermalis for bioremediation of high temperature radioactive waste environments. Appl. Environ. Microbiol. 69, 4575–4582 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Bik, E. M. et al. Molecular analysis of the bacterial microbiota in the human stomach. Proc. Natl Acad. Sci. USA 103, 732–737 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Daly, M. J. Modulating radiation resistance: insights based on defenses against reactive oxygen species in the radioresistant bacterium Deinococcus radiodurans. Clin. Lab. Med. 26, 491–504 (2006).

    Article  PubMed  Google Scholar 

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Acknowledgements

Work on protein oxidation in the Daly laboratory is supported by grant FA9550-07-1-0218 to M.J.D. from the Air Force Office of Scientific Research. The author thanks E.K. Gaidamakova and V.Y. Matrosova for assistance with the figures.

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  1. Michael J. Daly is at the Uniformed Services University of the Health Sciences, Bethesda, Maryland 20814, USA. mdaly@usuhs.edu mdaly@usuhs.mil,

    Michael J. Daly

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DATABASES

Entrez Genome Project

Bacillus pumilus

Caenorhabditis elegans

Deinococcus geothermalis

Deinococcus radiodurans

Escherichia coli

Halobacterium sp. NRC-1

Lactobacillus plantarum

Micrococcus luteus

Pyrococcus furiosus

Shewanella oneidensis

Synechocystis sp. PCC 68034

Ustilago maydis

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Daly, M. A new perspective on radiation resistance based on Deinococcus radiodurans. Nat Rev Microbiol 7, 237–245 (2009). https://doi.org/10.1038/nrmicro2073

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