Skip to main content
Log in

Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC1 to desiccation and gamma irradiation

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

We report that the halophilic archaeon Halobacterium sp. strain NRC-1 is highly resistant to desiccation, high vacuum and 60Co gamma irradiation. Halobacterium sp. was able to repair extensive double strand DNA breaks (DSBs) in its genomic DNA, produced both by desiccation and by gamma irradiation, within hours of damage induction. We propose that resistance to high vacuum and 60Co gamma irradiation is a consequence of its adaptation to desiccating conditions. Gamma resistance in Halobacterium sp. was dependent on growth stage with cultures in earlier stages exhibiting higher resistance. Membrane pigments, specifically bacterioruberin, offered protection against cellular damages induced by high doses (5 kGy) of gamma irradiation. High-salt conditions were found to create a protective environment against gamma irradiation in vivo by comparing the amount of DSBs induced by ionizing radiation in the chromosomal DNA of Halobacterium sp. to that of the more radiation-sensitive Escherichia coli that grows in lower-salt conditions. No inducible response was observed after exposing Halobacterium sp. to a nonlethal dose (0.5 kGy) of gamma ray and subsequently exposing the cells to either a high dose (5 kGy) of gamma ray or desiccating conditions. We find that the hypersaline environment in which Halobacterium sp. flourishes is a fundamental factor for its resistance to desiccation, damaging radiation and high vacuum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

DSBs:

Double-strand breaks

ROS:

Reactive oxygen species

EMS:

Ethyl methanesulfonate

Gy:

Gray

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(1):18–26

    Google Scholar 

  • Baliga NS, Bjork SJ, Bonneau R, Pan M, Iloanusi C, Kottemann MC, Hood L, DiRuggiero J (2004) Systems level insights into the stress response to UV radiation in the halophilic archaeon Halobacterium NRC −1. Genome Res 14(6):1025–1035 [Epub 2004 May 12]

    Google Scholar 

  • Battista JR, Earl AM, Park MJ (1999) Why is Deinococcus radiodurans so resistant to ionizing radiation? Trends Microbiol 7:362–365

    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(4):1489–1492

    Google Scholar 

  • Blaisdell JO, Wallace SS (2001) Abortive base-excision repair of radiation-induced clustered DNA lesions in Escherichia coli. PNAS USA 98(13):7426–7430

    Google Scholar 

  • Carbonneau MA, Melin AM, Perromat A, Clerc M (1989) The action of free radicals on Deinococcus radiodurans carotenoids. Arch Biochem Biophys 275(1):244–251

    Google Scholar 

  • Clavero MRS, Monk JD, Beuchat LR, Doyle MP, Brackett RE (1994) Inactivation of Escherichia coli 0157:H7, Salmonellae, and Campylobacter jejuni in raw ground beef by gamma irradiation. Appl Environ Microbiol 60(6):2069–2075

    Google Scholar 

  • Constantinesco F, Forterre P, Koonin E, Aravind L, Elie C (2004) A bipolar DNA helicase gene, herA, clusters with rad50, mre11 and nurA genes in thermophilic archaea. Nucleic Acids Res 32:1439–1447

    Google Scholar 

  • Crawford DR, Davies KJ (1994) Adaptive response and oxidative stress. Environ Health Perspect 102(Suppl)10:25–28

    Google Scholar 

  • Daly MJ, Ouyang L, Fuchs P, Minton KW (1994) In vivo damage and recA-dependent repair of plasmid and chromosomal DNA in the radiation-resistant bacterium Deinococcus radiodurans. J Bacteriol 176(12):3508–3517

    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) Sep 30 Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science [Epub ahead of print]

  • Della M, Palmbos PL, Tseng H-M, Tonkin LM, Daley JM, Topper LM, Pitcher RS, Tomkinson AE, Wilson TE, Doherty AJ (2004) Mycobacterial Ku and ligase proteins constitute a two-component NHEJ repair machine. Science 360:683–685

    Google Scholar 

  • 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

    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

    Google Scholar 

  • DiRuggiero J, Brown JR, Bogert AP, Robb FT (1999) DNA repair systems in Archaea: mementos from the last universal common ancestor? J Mol Evol 49:474–484

    Google Scholar 

  • Fish SA, Shepherd TJ, McGenity TJ, Grant WD (2002) Recovery of 16S ribosomal RNA gene fragments from ancient halite. Nature 417(6887):432–436

    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(1):72–78

    Google Scholar 

  • van Gerwen SJ, Rombouts FM, van’t Riet K, Zwietering MH (1999) A data analysis of the irradiation parameter D10 for bacteria and spores under various conditions. J Food Prot 62(9):1024–1032

    Google Scholar 

  • Gruber C, Legat A, Pfaffenhuemer M, Radax C, Weidler G, Hans-Jürgen B Helga S-L (2004) Halobacterium noricense sp. nov., an archaeal isolate from a bore core of an alpine Permian salt deposit, classification of Halobacterium sp. NRC-1 as a strain of H. salinarum and emended description of H. salinarum. Extremophiles [E-pub 30 July 2004]

  • Gutman PD, Carroll JD, Masters CI, Minton KW (1994) Sequencing, targeted mutagenesis and expression of a recA gene required for the extreme radioresistance of Deinococcus radiodurans. Gene 141:31–37

    Google Scholar 

  • Holden JF, Baross JA (1993) Enhanced thermotolerance and temperature-induced changes in protein composition in the hyperthermophilic archaeon ES4. J Bacteriol 175:2839–2843

    Google Scholar 

  • Hopfner KP, Karcher A, Shin D, Fairley C, Tainer JA, Carney JP (2000) Mre11 and Rad50 from Pyrococcus furiosus: cloning and biochemical characterization reveal an evolutionarily conserved multiprotein machine. J Bacteriol 182(21):6036–6041

    Google Scholar 

  • Hubmacher D, Matzanke BF, Anemuller S (2002) Investigations of iron uptake in Halobacterium salinarum. Biochem Soc Trans 4:710–712

    Google Scholar 

  • Jolivet E, L’Haridon S, Corre E, Forterre P, Prieur D (2003) Thermococcus gammatolerans sp. nov., a hyperthermophilic archaeon from a deep-sea hydrothermal vent that resists ionizing radiation. Int J Syst Evol Microbiol 53(3):847–851

    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(3):219–227. [Epub 2004 Feb 27]

    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(5):915-918

    Google Scholar 

  • Koike J, Oshima T, Koike KA, Taguchi H, Tanaka R, Nishimura K, Miyaji M (1992) Survival rates of some terrestrial microorganisms under high conditions. Adv Space Res 12(4):271–274

    Google Scholar 

  • Komori K, Miyata T, DiRuggiero J, Holley-Shanks R, Hayashi I, Cann IK, Mayanagi K, Shinagawa H, Ishino Y (2000a) Both RadA and RadB are involved in homologous recombination in Pyrococcus furiosus. J Biol Chem 275(43):33782–33790

    Google Scholar 

  • Komori K, Sakae S, Fujikane R, Morikawa K, Shinagawa H, Ishino Y (2000b) Biochemical characterization of the Hjc Holliday junction resolvase of Pyrococcus furiosus. Nucleic Acids Res 28(22):4544–4551

    Google Scholar 

  • Lanyi JK (1974) Salt-dependent properties of proteins from extremely halophilic bacteria. Bacteriol. Rev 38:272–290

    Google Scholar 

  • Makarova KS, Aravind L, Wolf YI, Tatusov RL, Minton KW, 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(1):44–79

    Google Scholar 

  • Mancinelli RL, White MR, Rothschild LJ (1998) Biopan-survival I: Exposure of the Osmophiles Synechococcus Sp. (Nageli) and Haloarcula Sp. to the space environment. Adv Space Res 22:327

    Google Scholar 

  • Marguet E, Forterre P (1998) Protection of DNA by salts against thermodegradation at temperatures typical for hyperthermophiles. Extremophiles 2(2):115–122

    Google Scholar 

  • Martin EL, Reinhardt RL, Baum LL, Becker MR, Shaffer JJ, Kokjohn TA (2000) The effects of ultraviolet radiation on the moderate halophile Halomonas elongata and the extreme halophile Halobacterium salinarum. Can J Microbiol 46(2):180–187

    Google Scholar 

  • Mattimore V, Battista JR (1996) Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol 178(3):633–637

    Google Scholar 

  • McCready S (1996) The repair of ultraviolet light-induced DNA damage in the halophilic archaebacteria, Halobacterium cutirubrum, Halobacterium halobium and Haloferax volcanii. Mutat Res 364(1):25–32

    Google Scholar 

  • McGenity TJ, Gemmell RT, Grant WD, Stan-Lotter H (2000) Origins of halophilic microorganisms in ancient salt deposits. Environ Microbiol 2(3):243–50

    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 17(5):457–464

    Google Scholar 

  • Moseley BEB (1983) Photobiology and radiobiology of Micrococcus (Deinococcus) radiodurans. Photochem Photobiol Rev 7:223–275

    Google Scholar 

  • Ng WL, Yang CF, Halladay JT, Arora P, DasSarma S (1995) Protocol 25: isolation of genomic and plasmid DNAs from Halobacterium halobium. In: Robb FT, Place AR, Sowers KR, Schreier HJ, DasSarma S, Fleischmann EM (eds) Archaea: a laboratory manual. Cold Spring Harbor Laboratory Press, Newyork pp 179–180

    Google Scholar 

  • Ng WV, Kennedy SP, Mahairas GG, Berquist B, Pan M, Shukla HD, Lasky SR, Baliga N, Thorsson V, Sbrogna J, Swartzell S, Weir D, Gall J, Dahl TA, Welti R, Goo YA, Leithauser B, Keller K, Cruz R, Danson MJ, Hough DW, Maddocks DG, Jablonski PE, Krebs MP, Angevine CM, Dale H, Isenbarger TA, Peck RF, Pohlschrod M, Spudich JL, Jung KH, Alam M, Freitas T, Hou S, Daniels CJ, Dennis PP, Omar AD, Ebhardt H, Lowe TM, Liang P, Riley M, Hood L, DasSarma S (1997) Genome sequence of Halobacterium species NRC-1. PNAS USA 22:12176–12181

    Google Scholar 

  • Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P (2000) Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol Mol Biol Rev 64(3):548–572

    Google Scholar 

  • Peck RF, DasSarma S, Krebs MP (2000) Homologous gene knockout in the archaeon Halobacterium salinarium with ura3 as a counterselectable marker. Mol Micro 35(3):667–676

    Google Scholar 

  • Potts M (1994) Desiccation tolerance of Prokaryotes. Microbiol Rev 58(4):755–805

    Google Scholar 

  • Rieder R, Gellert R, Anderson RC, Bruckner J, Clark BC, Dreibus G, Economou T, Klingelhofer G, Lugmair GW, Ming DW, Squyres SW, d’Uston C, Wanke H, Yen A, Zipfel J (2004) Chemistry of rocks and soils at Meridiani Planum from the alpha particle X-ray spectrometer. Science 306(5702):1746–1749

    Google Scholar 

  • Riley PA (1994) Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int J Radiat Biol 65(1):27–33

    Google Scholar 

  • Saffary R, Nandakumar R, Spencer D, Robb FT, Davila JM, Swartz M, Ofman L, Thomas RJ, DiRuggiero J (2002) Microbial survival of space vacuum and extreme ultraviolet irradiation: strain isolation and analysis during a rocket flight. FEMS Microbiol Lett 215(1):163–168

    Google Scholar 

  • Salin MN, Brown-Peterson NJ (1993) Dealing with active oxygen intermediates: a halophilic perspective. Experientia 49:523-529

    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 resistance of Halobacterium salinarium against DNA-damaging agents. J Radiat Res 39:251–262

    Google Scholar 

  • Trent JD, Gabrielsen M, Jensen B, Neuhard J, Olsen J (1994) Acquired thermotolerance and heat shock proteins in thermophiles from the three phylogenetic domains. J Bacteriol 176:6148–6152

    Google Scholar 

  • Ulsh BA, Miller SM, Mallory FF, Mitchel RE, Morrison DP, Boreham DR (2004) Cytogenetic dose–response and adaptive response in cells of ungulate species exposed to ionizing radiation. J Environ Radioact 74(1–3):73–81

    Google Scholar 

  • Vreeland RH, Rosenzweig WD (2002) The question of uniqueness of ancient bacteria. J Ind Microbiol Biotechnol 28(1):32–41

    Google Scholar 

Download references

Acknowledgements

This work was supported by grants from NASA (#NCC9147), and the HFSP (#RG522002). We would like to thank Vince Adams for his technical assistance irradiating the cells and Marvin Swartz for high vacuum exposure.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jocelyne DiRuggiero.

Additional information

Communicated by W.D. Grant

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kottemann, M., Kish, A., Iloanusi, C. et al. Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC1 to desiccation and gamma irradiation. Extremophiles 9, 219–227 (2005). https://doi.org/10.1007/s00792-005-0437-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-005-0437-4

Keywords

Navigation