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Deinococcus radiodurans: Revising the Molecular Basis for Radiation Effects on Cells

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Extremophiles Handbook

Abstract

The field of radiobiology was built on the premise that radiation is dangerous because of its damaging effects on DNA, where only a few events, or even a single event, at the molecular level can inactivate cells (Hutchinson 1966). The discordance of modern radiation toxicity models with results spanning nearly 5 decades of research on the extremely radiation-resistant bacterium Deinococcus radiodurans is reviewed. Much of the early data implicating DNA itself were for bacterial systems. However, recent studies show that extreme resistance to gamma radiation among bacteria consistently coincides with a greatly diminished susceptibility to protein oxidation but with similar DNA lesion-yields as other organisms. A growing body of experimental evidence now supports that naturally sensitive bacteria are killed by radiation mainly owing to protein oxidation, whereas extreme resistance in bacteria is achieved by protecting enzymes and the repair functions they catalyze. Based on new insights, the prospects for exporting the radioprotective mechanisms outside of D. radiodurans for practical purposes are considered.

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References

  • Akerlund T, Nordstrom K, Bernander R (1995) Analysis of cell size and DNA content in exponentially growing and stationary-phase batch cultures of Escherichia coli. J Bacteriol 177:6791–6797

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Anjem A, Varghese S, Imlay JA (2009) Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol Microbiol 72:844–858

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Barnese K, Gralla EB, Cabelli DE, Valentine JS (2008) Manganous phosphate acts as a superoxide dismutase. J Am Chem Soc 130:4604–4606

    Article  PubMed  CAS  Google Scholar 

  • Barron ES, Dickman S, Muntz JA, Singer TP (1949) Studies on the mechanism of action of ionizing radiations. II. Inhibition of sulfhydril enzymes by alpha, beta, and gamma rays. J Gen Physiol 32:537–552

    Article  PubMed  CAS  Google Scholar 

  • Battista JR (1997) Against all odds: the survival strategies of Deinococcus radiodurans. Ann Rev Microbiol 51:203–224

    Article  CAS  Google Scholar 

  • Berlett BS, Chock PB, Yim MB, Stadtman ER (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

    Article  PubMed  CAS  Google Scholar 

  • Billi D, Friedmann EI, Hofer KG, Caiola MG, Ocampo-Friedmann R (2000) Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol 66:1489–1492

    Article  PubMed  CAS  Google Scholar 

  • Blok J, Loman H (1973) The effects of γ-radiation in DNA. Curr Top Radiat Res Q 9:165–245

    PubMed  CAS  Google Scholar 

  • Bruce AK (1964) Extraction of the radioresistant factor of Micrococcus radiodurans. Radiat Res 22:155–164

    Article  PubMed  CAS  Google Scholar 

  • Dale WM (1940) The effect of X-rays on enzymes. Biochem J 34:1367–1373

    PubMed  CAS  Google Scholar 

  • Dale WM (1942) The effect of X-rays on the conjugated protein d-amino-acid oxidase. Biochem J 36:80–85

    PubMed  CAS  Google Scholar 

  • Dale WM (1943) Effects of X-rays on acetylcholine solutions showing the dilution and protection phenomena, found for enzymes. J Physiol 102:50–54

    PubMed  CAS  Google Scholar 

  • Daly MJ (2000) Engineering radiation-resistant bacteria for environmental biotechnology. Curr Opin Biotechnol 11:280–285

    Article  PubMed  CAS  Google Scholar 

  • Daly MJ (2009) A new perspective on radiation resistance based on Deinococcus radiodurans. Nat Rev Microbiol 7:237–245

    Article  PubMed  CAS  Google Scholar 

  • Daly MJ, Minton KW (1995) Interchromosomal recombination in the extremely radioresistant bacterium Deinococcus radiodurans. J Bacteriol 177:5495–5505

    PubMed  CAS  Google Scholar 

  • Daly MJ, Minton KW (1996) An alternative pathway of recombination of chromosomal fragments precedes recA-dependent recombination in the radioresistant bacterium Deinococcus radiodurans. J Bacteriol 178:4461–4471

    PubMed  CAS  Google Scholar 

  • Daly MJ, Minton KW (1997) Recombination between a resident plasmid and the chromosome following irradiation of the radioresistant bacterium Deinococcus radiodurans. Gene 187:225–229

    Article  PubMed  CAS  Google Scholar 

  • Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Venkateswaran A, Hess M, Omelchenko MV, Kostandarithes HM, Makarova KS, Wackett LP, Fredrickson JK, Ghosal D (2004) Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306:1025–1028

    Article  PubMed  CAS  Google Scholar 

  • Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Leapman RD, Lai B, Ravel B, Li SM, Kemner KM, Fredrickson JK (2007) Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol 5:769–779

    Article  CAS  Google Scholar 

  • Daly MJ, Gaidamakova EK, Matrosova VY, Kiang JG, Fukumoto R, Lee DY, Wehr NB, Viteri GA, Berlett BS, Levine RL (2010) Small-molecule antioxidant proteome-shields in Deinococcus radiodurans PLoS One 5(9):e12570

    Google Scholar 

  • Datta SK, Okamoto S, Hayashi T, Shin SS, Mihajlov I, Fermin A, Guiney DG, Fierer J, Raz E (2006) Vaccination with irradiated Listeria induces protective T cell immunity. Immunity 25(1):143–152

    Article  PubMed  CAS  Google Scholar 

  • Davies R, Sinskey AJ (1973) Radiation-resistant mutants of Salmonella typhimurium LT2: development and characterization. J Bacteriol 113:133–144

    PubMed  CAS  Google Scholar 

  • de Groot A, Chapon V, Servant P, Christen R, Saux MF, Sommer S, Heulin T (2005) Deinococcus deserti sp. nov., a gamma-radiation-tolerant bacterium isolated from the Sahara Desert. Int J Syst Evol Microbiol 55:2441–2446

    Article  PubMed  Google Scholar 

  • Du J, Gebicki J (2004) Proteins are major initial cell targets of hydroxyl free radicals. Int J Biochem Cell Biol 36:2334–2343

    Article  PubMed  CAS  Google Scholar 

  • Eisenstadt E, Fisher S, Der CL, Silver S (1973) Manganese transport in Bacillus subtilis W23 during growth and sporulation. J Bacteriol 113:1363–1372

    PubMed  CAS  Google Scholar 

  • Erdman IE, Thatcher FS, Macqueen KF (1961) Studies on the irradiation of microorganisms in relation to food preservation. II. Irradiation resistant mutants. Can J Microbiol 7:207–215

    Article  PubMed  CAS  Google Scholar 

  • Ferreira AC, Nobre MF, Rainey FA, Silva MT, Wait R, Burghardt J, Chung AP, da Costa MS (1997) 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

    Article  PubMed  CAS  Google Scholar 

  • Gérard E, Jolivet E, Prieur D, 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

    Article  PubMed  Google Scholar 

  • Ghosal D, Omelchenko MV, Gaidamakova EK, Matrosova VY, Vasilenko A, Venkateswaran A, Zhai M, Kostandarithes HM, Brim H, Makarova KS, Wackett LP, Fredrickson JK, Daly MJ (2005) How radiation kills cells: survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress. FEMS Microbiol Rev 29:361–375

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Glasser O (1993) Wilhelm Conrad Röntgen and the early history of the Roentgen rays. Norman Publishing Division of Jeremy Morman, San Francisco

    Google Scholar 

  • Goodarzi AA, Noon AT, Jeggo PA (2009) The impact of heterochromatin on DSB repair. Biochem Soc Trans 37:569–576

    Article  PubMed  CAS  Google Scholar 

  • Hansen MT (1978) Multiplicity of genome equivalents in the radiation-resistant bacterium Micrococcus radiodurans. J Bacteriol 134:71–75

    PubMed  CAS  Google Scholar 

  • Harris DR, Pollock SV, Wood EA, Goiffon RJ, Klingele AJ, Cabot EL, Schackwitz W, Martin J, Eggington J, Durfee TJ, Middle CM, Norton JE, Popelars MC, Li H, Klugman SA, Hamilton LL, Bane LB, Pennacchio LA, Albert TJ, Perna NT, Cox MM, Battista JR (2009) Directed evolution of ionizing radiation resistance in Escherichia coli. J Bacteriol 191:5240–5252

    Article  PubMed  CAS  Google Scholar 

  • Holloman WK, Schirawski J, Holliday R (2007) Towards understanding the extreme radiation resistance of Ustilago maydis. Trends Microbiol 15:525–529

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Kevles BH (1997) Naked to the bone: medical imaging in the twentieth century. Rutgers University Press, New Brunswick

    Google Scholar 

  • Kota S, Misra HS (2006) PprA: A protein implicated in radioresistance of Deinococcus radiodurans stimulates catalase activity in Escherichia coli. Appl Microbiol Biotechnol 72:790–796

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Krisch RE, Flick MB, Trumbore CN (1991) Radiation chemical mechanisms of single-and double-strand break formation in irradiated SV40 DNA. Radiat Res 126:251–259

    Google Scholar 

  • Kriško A, Radman M (2010) Protein damage and death by radiation in Escherichia coli and Deinococcus radiodurans. Proc Natl Acad Sci USA. (www.pnas.org/cgi/doi/10.1073/pnas.100931.2107)

    Google Scholar 

  • Leibowitz PJ, Schwartzberg LS, Bruce AK (1976) The in vivo association of manganese with the chromosome of Micrococcus radiodurans. Photochem Photobiol 23:45–50

    Article  PubMed  CAS  Google Scholar 

  • Levine RL, Stadtman ER (2001) Oxidative modification of proteins during aging. Exp Gerontol 36:1495–1502

    Article  PubMed  CAS  Google Scholar 

  • Levinson HS, Hyatt MT (1960) Some effects of heat and ionizing radiation on spores of Bacillus megaterium. J Bacteriol 80:441–451

    PubMed  CAS  Google Scholar 

  • Lin J, Qi R, Aston C, Jing J, Anantharaman TS, Mishra B, White O, Daly MJ, Minton KW, Venter JC, Schwartz DC (1999) Whole-genome shotgun optical mapping of Deinococcus radiodurans. Science 285:1558–1562

    Article  PubMed  CAS  Google Scholar 

  • Makarova KS, Daly MJ (2010) Comparative genomics of stress response systems in Deinococcus bacteria. In: Storz G, Hennge R (eds) Bacterial stress responses. ASM Press, Washington, DC

    Google Scholar 

  • Makarova KS, Aravind L, Wolf YI, Tatusov RL, Minton K, Koonin EV, Daly MJ (2001) Genome of the extremely radiation resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol Mol Biol Rev 65:44–79

    Article  PubMed  CAS  Google Scholar 

  • Minton KW (1994) DNA repair in the extremely radioresistant bacterium Deinococcus radiodurans. Mol Microbiol 13:9–15

    Article  PubMed  CAS  Google Scholar 

  • Minton KW (1996) Repair of ionizing-radiation damage in the radiation resistant bacterium Deinococcus radiodurans. Mutat Res 363:1–7

    Article  PubMed  Google Scholar 

  • Minton KW, Daly MJ (1995) A model for repair of radiation-induced DNA double-strand breaks in the extreme radiophile Deinococcus radiodurans. Bioessays 7:457–464

    Article  Google Scholar 

  • Moseley BE, Mattingly A (1971) Repair of irradiation transforming deoxyribonucleic acid in wild type and a radiation-sensitive mutant of Micrococcus radiodurans. J Bacteriol 105:976–983

    PubMed  CAS  Google Scholar 

  • Mould RF (1993) A century of X-rays and radioactivity in medicine. Institute of Physics Publishing, London

    Google Scholar 

  • Norais CA, Chitteni-Pattu S, Wood EA, Inman RB, Cox MM (2009) DdrB protein, an alternative Deinococcus radiodurans SSB induced by ionizing radiation. J Biol Chem 284:21402–21411

    Article  PubMed  CAS  Google Scholar 

  • Omelchenko MV, Wolf YI, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Daly MJ, Koonin EV, Makarova KS (2005) Comparative genomics of Thermus thermophilus and Deinococcus radiodurans: divergent routes of adaptation to thermophily and radiation resistance. BMC Evol Biol 5:57–80

    Article  PubMed  Google Scholar 

  • Parisi A, Antoine AD (1974) Increased radiation resistance of vegetative Bacillus pumilus. Appl Microbiol 28:41–46

    PubMed  CAS  Google Scholar 

  • Rothkamm K, Löbrich M (2003) Evidence for a lack of DNA double-strand break repair in human cells exposed to very low X-ray doses. Proc Natl Acad Sci USA 100:5057–5062

    Google Scholar 

  • Scott CM (1937) Some quantitative aspects of the biological actions of X and γ rays. Great Britain Medical Research Council, Special Report Series, No. 223:5–99

    Google Scholar 

  • Setlow P (2007) I will survive: DNA protection in bacterial spores. Trends Microbiol 15:172–180

    Article  PubMed  CAS  Google Scholar 

  • Shirkey B, McMaster NJ, Smith SC, Wright DJ, Rodriguez H, Jaruga P, Birincioglu M, Helm RF, Potts M (2003) 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

    Article  PubMed  CAS  Google Scholar 

  • Shuryak I, Brenner DJ (2009) A model of interactions between radiation-induced oxidative stress, protein and DNA damage in Deinococcus radiodurans. J Theor Biol 261:305–317

    Article  PubMed  CAS  Google Scholar 

  • Thornley MJ (1963) Radiation resistance among bacteria. J Appl Bacteriol 26:334–345

    Article  Google Scholar 

  • von Sonntag C (1987) The chemical basis of radiation biology. Taylor & Francis, London

    Google Scholar 

  • Zhang SH, Hou SG, Yang GL, Wang JH (2009) Bacterial community in the East Rongbuk Glacier, Mt. Qomolangma (Everest) by culture and culture-independent methods. Microbiol Res 165:336–345

    Google Scholar 

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Acknowledgment

The work of M.J. Daly is supported by the Air Force Office of Scientific Research.

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Correspondence to Michael J. Daly .

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Daly, M.J. (2011). Deinococcus radiodurans: Revising the Molecular Basis for Radiation Effects on Cells. In: Horikoshi, K. (eds) Extremophiles Handbook. Springer, Tokyo. https://doi.org/10.1007/978-4-431-53898-1_53

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