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Recovery of ionizing-radiation damage after high doses of gamma ray in the hyperthermophilic archaeon Thermococcus gammatolerans

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Abstract

The recently discovered hyperthermophilic and radioresistant archaeon Thermococcus gammatolerans is of great interest to compare and contrast the impact of its physiology on radioresistance and its ability to repair damaged chromosomes after exposure to gamma irradiation with radioresistant bacteria. We showed that, in contrast to other organisms, cell survival was not modified by the cellular growth phase under optimal growth conditions but nutrient-limited conditions did affect the T. gammatolerans radioresistance. We determined the first kinetics of damaged DNA recovery in an archaeon after exposure to massive doses of gamma irradiation and compared the efficiency of chromosomal DNA repair according to the cellular growth phase, nutrient availability and culture conditions. Chromosomal DNA repair kinetics showed that stationary phase cells reconstitute disrupted chromosomes more rapidly than exponential phase cells. Our data also revealed that this radioresistant archaeon was proficient to reconstitute shattered chromosomes either slowly or rapidly without any loss of viability. These results suggest that rapid DNA repair is not required for the extreme radioresistance of T. gammatolerans.

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References

  • Bala M, Jain V (1996) 2-DG induced modulation of chromosomal DNA profile, cell survival, mutagenesis and gene conversion in X-irradiated yeast. Indian J Exp Biol 34:18–26

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bentchikou E, Servant P, Coste G, Sommer S (2007) Additive effects of SbcCD and PolX deficiencies in the in vivo repair of DNA double-strand breaks in Deinococcus radiodurans. J Bacteriol 189:4784–4790

    Article  PubMed  CAS  Google Scholar 

  • Bernander R (2003) The archaeal cell cycle: current issues. Mol Microbiol 48:599–604

    Article  PubMed  CAS  Google Scholar 

  • Breuert S, Allers T, Spohn G, Soppa J (2006) Regulated polyploidy in halophilic archaea. PLoS ONE 1:e92

    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:e92

    Article  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  CAS  Google Scholar 

  • Dinger ME, Baillie GJ, Musgrave DR (2000) Growth phase-dependent expression and degradation of histones in the thermophilic archaeon Thermococcus zilligii. Mol Microbiol 36:876–885

    Article  PubMed  CAS  Google Scholar 

  • Dion P, Charbonneau R, Thibault C (1994) Effect of ionizing dose rate on the radioresistance of some food pathogenic bacteria. Can J Microbiol 40:369–374

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Gerard 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  CAS  Google Scholar 

  • Jolivet E, L’Haridon S, Corre E, Forterre P, 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

    Article  PubMed  CAS  Google Scholar 

  • Jolivet E, Matsunaga F, Ishino Y, Forterre P, Prieur D, Myllykallio H (2003b) Physiological responses of the hyperthermophilic archaeon “Pyrococcus abyssi” to DNA damage caused by ionizing radiation. J Bacteriol 185:3958–3961

    Article  PubMed  CAS  Google Scholar 

  • Jolivet E, Corre E, L’Haridon S, Forterre P, Prieur D (2004) Thermococcus marinus sp. nov. and Thermococcus radiotolerans sp. nov., two hyperthermophilic archaea from deep-sea hydrothermal vents that resist ionizing radiation. Extremophiles 8:219–227

    Article  PubMed  CAS  Google Scholar 

  • Keller LC, Maxcy RB (1984) Effect of physiological age on radiation resistance of some bacteria that are highly radiation resistant. Appl Environ Microbiol 47:915–918

    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 

  • Krasin F, 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

    Article  PubMed  CAS  Google Scholar 

  • Majernik AI, Lundgren M, McDermott P, Bernander R, Chong JP (2005) DNA content and nucleoid distribution in Methanothermobacter thermautotrophicus. J Bacteriol 187:1856–1858

    Article  PubMed  CAS  Google Scholar 

  • Makarova KS, Omelchenko MV, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Lapidus A, Copeland A, Kim E, Land M, Mavrommatis K, Pitluck S, Richardson PM, Detter C, Brettin T, Saunders E, Lai B, Ravel B, Kemner KM, Wolf YI, Sorokin A, Gerasimova AV, Gelfand MS, Fredrickson JK, Koonin EV, Daly MJ (2007) Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks. PLoS ONE 2:e955

    Article  PubMed  CAS  Google Scholar 

  • Minsky A (2003) Structural aspects of DNA repair: the role of restricted diffusion. Mol Microbiol 50:367–376

    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 

  • Riley PA (1994) Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int J Radiat Biol 65:27–33

    Article  PubMed  CAS  Google Scholar 

  • Sato T, Fukui T, Atomi H, Imanaka T (2003) Targeted gene disruption by homologous recombination in the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1. J Bacteriol 185:210–220

    Article  PubMed  CAS  Google Scholar 

  • Shahmohammadi HR, Asgarani E, Terato H, Saito T, Ohyama Y, Gekko K, Yamamoto O, Ide H (1998) Protective roles of bacterioruberin and intracellular KCl in the resistance of Halobacterium salinarium against DNA-damaging agents. J Radiat Res (Tokyo) 39:251–262

    Article  CAS  Google Scholar 

  • White O, Eisen JA, Heidelberg JF, Hickey EK, Peterson JD, Dodson RJ, Haft DH, Gwinn ML, Nelson WC, Richardson DL, Moffat KS, Qin H, Jiang L, Pamphile W, Crosby M, Shen M, Vamathevan JJ, Lam P, McDonald L, Utterback T, Zalewski C, Makarova KS, Aravind L, Daly MJ, Minton KW, Fleischmann RD, Ketchum KA, Nelson KE, Salzberg S, Smith HO, Venter JC, Fraser CM (1999) Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science 286:1571–1577

    Article  PubMed  CAS  Google Scholar 

  • Williams E, Lowe TM, Savas J, DiRuggiero J (2007) Microarray analysis of the hyperthermophilic archaeon Pyrococcus furiosus exposed to gamma irradiation. Extremophiles 11:19–29

    Article  PubMed  CAS  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87:4576–4579

    Article  PubMed  CAS  Google Scholar 

  • Zahradka K, Slade D, Bailone A, Sommer S, Averbeck D, Petranovic M, Lindner AB, Radman M (2006) Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature 443:569–573

    PubMed  CAS  Google Scholar 

  • Zimmerman JM, Battista JR (2005) A ring-like nucleoid is not necessary for radioresistance in the Deinococcaceae. BMC Microbiol 5:17

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The LGA laboratory is supported by the CNRS and the Université Paris-Sud XI. A. Tapias was the recipient of an ATER-Université Paris-Sud XI position in Molecular Biology. C. Leplat is supported by a doctoral fellowship of the Ecole Doctorale GCDE Paris- Sud XI. Authors are specially grateful to J. Battista (Lousiana State University, USA) for fruitful discussions. We thank P. Forterre and E. Marguet for their help in the use of the anaerobic chamber and M. DuBow for help with English. We also thank G. Baldacci and V. Favaudon (Institut Curie, Orsay) for access to the Cs137 Gamma irradiation source. Authors are grateful to anonymous reviewers for their questions and suggestions to improve the quality of the manuscript.

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  1. Angels Tapias

    Present address: Departamento de Biotecnología Microbiana, Centro Nacional de Biotecnología, CNB, CSIC, Madrid, Spain

Authors and Affiliations

  1. Laboratoire de Génomique des Archaea, Université Paris-Sud 11 CNRS UMR 8621, Institut de Génétique et Microbiologie, Orsay, France

    Angels Tapias, Christophe Leplat & Fabrice Confalonieri

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  1. Angels Tapias
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  2. Christophe Leplat
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  3. Fabrice Confalonieri
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Correspondence to Fabrice Confalonieri.

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Communicated by H. Santos.

Angels Tapias and Christophe Leplat contributed equally to this work.

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Tapias, A., Leplat, C. & Confalonieri, F. Recovery of ionizing-radiation damage after high doses of gamma ray in the hyperthermophilic archaeon Thermococcus gammatolerans . Extremophiles 13, 333–343 (2009). https://doi.org/10.1007/s00792-008-0221-3

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