Advertisement

Extremophiles

, Volume 11, Issue 1, pp 19–29 | Cite as

Microarray analysis of the hyperthermophilic archaeon Pyrococcus furiosus exposed to gamma irradiation

  • Ernest Williams
  • Todd M. Lowe
  • Jeffrey Savas
  • Jocelyne DiRuggiero
Original Paper

Abstract

The remarkable survival of the hyperthermophilic archaeon Pyrococcus furiosus to ionizing radiation was previously demonstrated. Using a time course study and whole-genome microarray analyses of mRNA transcript levels, the genes and regulatory pathways involved in the repair of lesions produced by ionizing irradiation (oxidative damage and DNA strand breaks) in P. furiosus were investigated. Data analyses showed that radA, encoding the archaeal homolog of the RecA/Rad51 recombinase, was moderately up regulated by irradiation and that a putative DNA-repair gene cluster was specifically induced by exposure to ionizing radiation. This novel repair system appears to be unique to thermophilic archaea and bacteria and is suspected to be involved in translesion synthesis. Genes that encode for a putative Dps-like iron-chelating protein and two membrane-bound oxidoreductases were differentially expressed following gamma irradiation, potentially in response to oxidative stress. Surprisingly, the many systems involved in oxygen detoxification and redox homeostasis appeared to be constitutively expressed. Finally, we identified several transcriptional regulators and protein kinases highly regulated in response to gamma irradiation.

Keywords

Archaea Hyperthermophile DNA repair Ionizing radiation Oxidative stress Transcriptional analysis 

Notes

Acknowledgments

We thank Peter Kennelly for help in analyzing the protein kinase sequences from P. furiosus, and Rhonda Holley-shank for technical support. This work was supported by funds from NASA (NCC9147 to JDR) and the Human Frontier Science Program (RG522002 to JDR).

Supplementary material

792_2006_2_MOESM1_ESM.pdf (228 kb)
Supplementary material

References

  1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  2. Baliga NS, Bjork SJ, Bonneau R, Pan M, Iloanusi C, Kottemann MCH, Hood L, DiRuggiero J (2004) Systems level insights into the stress response to UV radiation in the halophilic archaeon Halobacterium NRC-1. Genome Res 14:1025–1035PubMedCrossRefGoogle Scholar
  3. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL (2002) The Pfam protein families database. Nucleic Acids Res 30:276–280PubMedCrossRefGoogle Scholar
  4. Bell SD, Cairns SS, Robson RL, Jackson SP (1999) Transcriptional regulation of an archaeal operon in vivo and in vitro. Mol Cell 4:971–982PubMedCrossRefGoogle Scholar
  5. Brinkman AB, Dahlke I, Tuininga JE, Lammers T, Dumay V, de Heus E, Lebbink JH, Thomm M, de Vos WM, van Der Oost J (2000) An Lrp-like transcriptional regulator from the archaeon Pyrococcus furiosus is negatively autoregulated. J Biol Chem 275:38160–38169PubMedCrossRefGoogle Scholar
  6. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal Biochem 162:156–159PubMedCrossRefGoogle Scholar
  7. Christendat D, Yee A, Dharamsi A, Kluger Y, Savchenko A, Cort JR, Booth V, Mackereth CD, Saridakis V, Ekiel I, Kozlov G, Maxwell KL, Wu N, McIntosh LP, Gehring K, Kennedy MA, Davidson AR, Pai EF, Gerstein M, Edwards AM, Arrowsmith CH (2000) Structural proteomics of an archaeon. Nat Struct Biol 7:903–909PubMedCrossRefGoogle Scholar
  8. Corpet F, Servant F, Gouzy J, Kahn D (2000) ProDom and ProDom-CG: tools for protein domain analysis and whole genome comparisons. Nucleic Acids Res 28:267–269PubMedCrossRefGoogle Scholar
  9. Courcelle J, Khodursky A, Peter B, Brown PO, Hanawalt PC (2001) Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics 158:41–64PubMedGoogle Scholar
  10. Cox MM, Battista JR (2005) Deinococcus radiodurans—the consumate survivor. Nature Rev Microbiol 3:882–892CrossRefGoogle Scholar
  11. Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Venkateswaran A, Hess M, Omelchenko MV, Kostandarithes H M, Makarova KS, Wackett LP, Fredrickson JK, Ghosal D (2004) Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306:1025–1028PubMedCrossRefGoogle Scholar
  12. Deppenmeier U (2002) The unique biochemistry of methanogenesis. Prog Nucleic Acid Res Mol Biol 71:223–283PubMedGoogle Scholar
  13. Dianov GL, O’Neill P, Goodhead DT (2001) Securing genome stability by orchestrating DNA repair: removal of radiation clustered leions in DNA. Bioessays 23:745–749PubMedCrossRefGoogle Scholar
  14. 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 179:4643–4645PubMedGoogle Scholar
  15. DiRuggiero J, Robb FT (2004) Early evolution of DNA repair mechanisms. In: Ribas de Pouplana L (eds) The genetic code, the origin of life. Landes Biosciences pp 474–485Google Scholar
  16. Eichler J, Adams MWW (2005) Posttranslational protein modification in archaea. Microbiol Mol Biol Rev 69:393–425PubMedCrossRefGoogle Scholar
  17. Fiala G, Stetter KO (1986) Pyrococcus furiosus sp. nov. represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100°C. Arch Microbiol 145:56–61CrossRefGoogle Scholar
  18. Fournier M, Dermoun Z, Durand MC, Dolla A (2004) A new function of the Desulfovibrio vulgaris Hildenborough [Fe] hydrogenase in the protection against oxidative stress. J Biol Chem 279:1787–1793PubMedCrossRefGoogle Scholar
  19. Friedberg EC, Walker GC, Siede W (1995) DNA repair and mutagenesis. ASM, WashingtonGoogle Scholar
  20. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241–4257PubMedGoogle Scholar
  21. Geer LY, Domrachev M, Lipman DJ, Bryant SH (2002) CDART: protein homology by domain architecture. Genome Res 12:1619–1623PubMedCrossRefGoogle Scholar
  22. 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 Genom 266:72–78CrossRefGoogle Scholar
  23. Golden MH, Ramdath D (1987) Free radicals in the pathogenesis of kwashiorkor. Proc Nutr Soc 46:53–68PubMedCrossRefGoogle Scholar
  24. Grogan DW (2004) Stability and repair of DNA in hyperthermophilic archaea. Curr Issues Mol Biol 6:137–144PubMedGoogle Scholar
  25. Guy CP, Haldenby S, Brindley A, Walsh DA, Briggs GS, Warren MJ, Allers T, Bolt EL (2006) Interactions of RadB, a DNA repair protein in archaea, with DNA and ATP. J Mol Biol 358:46–56PubMedCrossRefGoogle Scholar
  26. Hanks SK, Hunter T (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9:576–596PubMedGoogle Scholar
  27. Harris DR, Ward DE, Feasel JM, Lancaster KM, Murphy RD, Mallet TC, Crane III EJ (2005) Discovery and characterization of a Coenzyme A disulfide reductase from Pyrococcus horikoshii. FEBS J 272:1189–1200PubMedCrossRefGoogle Scholar
  28. Hutchinson F (1985) Chemical changes induced in DNA by ionizing radiation. Prog Nucl Acid Res Mol Biol 32:115–154CrossRefGoogle Scholar
  29. Ideker T, Thorsson V, Siegel AF, Hood LE (2000) Testing for differentially-expressed genes by maximum-likelihood analysis of microarray data. J Comput Biol 7:805–817PubMedCrossRefGoogle Scholar
  30. Imlay JA (2003) Pathways of oxidative damage. Ann Rev Microbiol 57:395–418CrossRefGoogle Scholar
  31. Ishino Y, Nishino T, Morikawa K (2006) Mechanisms of maintaining genetic stability by homologous recombination. Chem Rev 106:324–339PubMedCrossRefGoogle Scholar
  32. Jolivet E, Matsunaga F, Ishino Y, Forterre P, Prieur D, Myllykallio H (2003) Physiological responses of the hyperthermophilic archaeon “Pyrococcus abyssi” to DNA damage caused by ionizing radiation. J Bacteriol 185:3958–3961PubMedCrossRefGoogle Scholar
  33. Kawakami R, Sakuraba H, Kamohara S, Goda S, Kawarabayasi Y, Ohshima T (2004) Oxidative stress response in an anaerobic hyperthermophilic archaeon: presence of a functional peroxiredoxin in Pyrococcus horikoshii. J Biochem 136:541–547PubMedCrossRefGoogle Scholar
  34. Kelman Z, White MF (2005) Archaeal DNA replication and repair. Curr Opin Microbiol 8:669–676PubMedCrossRefGoogle Scholar
  35. Kennelly PJ (2003) Archaeal protein kinases and protein phosphatases: insights from genomics and biochemistry. Biochem J 370:373–389PubMedCrossRefGoogle Scholar
  36. Khil PP, Camerini-Otero RD (2002) Over 1000 genes are involved in the DNA damage response of Escherichia coli. Mol Microbiol 44:89–105PubMedCrossRefGoogle Scholar
  37. Komori K, Miyata T, DiRuggiero J, Holley-Shanks R, Hayashi I, Cann I K, Mayanagi K, Shinagawa H, Ishino Y (2000) Both RadA and RadB are involved in homologous recombination in Pyrococcus furiosus. J Biol Chem 275:33782–33790PubMedCrossRefGoogle Scholar
  38. 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 9:219–227PubMedCrossRefGoogle Scholar
  39. Kultz D (2005) Molecular and evolutionary basis of the cellular stress response. Ann Rev Physiol. 67:225–257CrossRefGoogle Scholar
  40. Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32:D142–D144PubMedCrossRefGoogle Scholar
  41. Limauro D, Pedone E, Pirone L, Bartolucci S (2006) Identification and characterization of 1-Cys peroxiredoxin from Sulfolobus solfataricus and its involvement in the response to oxidative stress. FEBS J 273:721–731PubMedCrossRefGoogle Scholar
  42. Liu Y, Zhou J, Omelchenko MV, Beliaev AS, Venkateswaran A, Stair J, Wu L, Thompson DK, Xu D, Rogozin IB, Gaidamakova EK, Zhai M, Makarova KS, Koonin EV, Daly MJ (2003) Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc Natl Acad Sci USA 100:4191–4196PubMedCrossRefGoogle Scholar
  43. Lucas S, Toffin L, Zivanovic Y, Charlier D, Moussard H, Forterre P, Prieur D, Erauso G (2002) Construction of a shuttle vector for, and spheroplast transformation of, the hyperthermophilic archaeon Pyrococcus abyssi. Appl Environ Microbiol 68:5528–5536PubMedCrossRefGoogle Scholar
  44. Ma K, Weiss R, Adams MW (2000) Characterization of hydrogenase II from the hyperthermophilic archaeon Pyrococcus furiosus and assessment of its role in sulfur reduction. J Bacteriol 182:1864–1871PubMedCrossRefGoogle Scholar
  45. Maeder DL, Weiss RB, Dunn DM, Cherry JL, Gonzalez JM, DiRuggiero J, Robb FT (1999) Divergence of the hyperthermophilic archaea Pyrococcus furiosus and P. horikoshii inferred from complete genomic sequences. Genetics 152:1299–1305PubMedGoogle Scholar
  46. Makarova KS, Aravind L, Grishin NV, Rogozin IB, Koonin EV (2002) A DNA repair system specific for thermophilic Archaea and bacteria predicted by genomic context analysis. Nucleic Acids Res 30:482–496PubMedCrossRefGoogle Scholar
  47. Marchler-Bauer A, Anderson JB, Cherukuri PF, DeWeese-Scott C, Geer LY, Gwadz M, He S, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Liebert CA, Liu C, Lu F, Marchler GH, Mullokandov M, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Yamashita RA, Yin JJ, Zhang D, Bryant S H (2005) CDD: a conserved domain database for protein classification. Nucleic Acids Res 33:D192–D196PubMedCrossRefGoogle Scholar
  48. Ouhammouch M, Werner F, Weinzierl ROJ, Geiduschek EP (2004) A fully recombinant system for activator-dependent archaeal transcription. J Biol Chem 279:51719–51721PubMedCrossRefGoogle Scholar
  49. Peak JG, Ito T, Robb FT, Peak MJ (1995) DNA damage produced by exposure of supercoiled plasmid DNA to high- and low-LET ionizind radiation: effects of hydroxyl radical quenchers. Int J Radiat Biol 67:1–6PubMedCrossRefGoogle Scholar
  50. Praul CA, Taylor WD (1997) Responses of Halobacterium halobium and Sulfolobus solfataricus to hydrogen peroxide and N-methyl-N′-nitro-N-nitrosoguanidine [correction of N-methyl-N-nitrosoguanidine] exposure. Microbiol Res 152:257–260Google Scholar
  51. Pulliainen AT, Kauko A, Haataja S, Papageorgiou AC, Finne J (2005) Dps/Dpr ferritin-like protein: insights into the mechanism of iron incorporation and evidence for a central role in cellular iron homeostasis in Streptococcus suis. Mol Microbiol 57:1086–1100PubMedCrossRefGoogle Scholar
  52. Ramsay B, Wiedenheft B, Allen M, Gauss GH, Martin Lawrence C, Young M, Douglas T (2006) Dps-like protein from the hyperthermophilic archaeon Pyrococcus furiosus. J Inorg Biochem 100(5–6):1061–1068PubMedCrossRefGoogle Scholar
  53. Reich CI, McNeil LK, Brace JL, Brucker JK, Olsen GJ (2001) Archaeal RecA homologues: different response to DNA-damaging agents in mesophilic and thermophilic Archaea. Extremophiles 5:265–275PubMedCrossRefGoogle Scholar
  54. Riley PA (1994) Free radicals in biology:oxidative stress and the effects of ionizing radiation. Int J Radiat Biol 65:27–33PubMedCrossRefGoogle Scholar
  55. Robb FT, Park JB, Adams MWW (1992) Characterization of an extremely thermostable glutamate dehydrogenase: a key enzyme in the primary metabolism of the hyperthermophilic archaebacterium Pyrococcus furiosus. Biochim Biophys Acta 1120:267–272PubMedGoogle Scholar
  56. Rohlin L, Trent JD, Salmon K, Kim U, Gunsalus RP, Liao JC (2005) Heat shock response of Archaeoglobus fulgidus. J Bacteriol 187:6046–6057PubMedCrossRefGoogle Scholar
  57. Salerno V, Napoli A, White MF, Rossi M, Ciaramella M (2003) Transcriptional response to DNA damage in the archaeon Sulfolobus solfataricus. Nucl Acids Res 31:6127–6138PubMedCrossRefGoogle Scholar
  58. Sapra R, Verhagen MFJM, Adams MWW (2000) Purification and characterization of a membrane-bound hydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 182:3423–3428PubMedCrossRefGoogle Scholar
  59. Schut GJ, Zhou J, Adams MWW (2001) DNA microarray analysis of the hyperthermophilic archaeon Pyrococcus furiosus: evidence for a new type of sulfur-reducing enzyme complex. J Bacteriol 183:7027–7036PubMedCrossRefGoogle Scholar
  60. Schut GJ, Brehm SD, Datta S, Adams MWW (2003) Whole-genome DNA microarray analysis of a hyperthermophile and an archaeon: Pyrococcus furiosus grown on carbohydrates or peptides. J Bacteriol 185:3935–3947PubMedCrossRefGoogle Scholar
  61. Shockley KR, Ward DE, Chhabra SR, Conners SB, Montero CI, Kelly RM (2003) Heat shock response by the hyperthermophilic archaeon Pyrococcus furiosus. Appl Environ Microbiol 69:2365–2371PubMedCrossRefGoogle Scholar
  62. Silva PJ, van den Ban ECD, Wassink H, Haaker H, de Castro B, Robb FT, Hagen WR (2000) Enzymes of hydrogen metabolism in Pyrococcus furiosus. Eur J Biochem 267:6541–6551PubMedCrossRefGoogle Scholar
  63. Tahara M, Ohsawa A, Saito S, Kimura M (2004) In vitro phosphorylation of initiation factor 2 alpha (aIF2 alpha) from hyperthermophilic archaeon Pyrococcus horikoshii OT3. J Biochem (Tokyo) 135:479–485Google Scholar
  64. Tatur J, Hagedoorn P-L, Overeijnder ML, Hagen WR (2005) A highly thermostable ferritin from the hyperthermophilic archaeal anaerobe Pyrococcus furiosus. Extremophiles 10(2):139–148PubMedCrossRefGoogle Scholar
  65. Theil EC (1987) Ferritin: structure, gene regulation, and cellular function in animals, plants, and microorganisms. Annu Rev Biochem 56:289–315PubMedCrossRefGoogle Scholar
  66. Van Ooteghem SA, Beer SK, Yue PC (2002) Hydrogen production by the thermophilic bacterium Thermotoga neapolitana. Appl Biochem Biotechnol 98–100:177–189PubMedCrossRefGoogle Scholar
  67. Vignais P, Colbeau A (2004) Molecular biology of microbial hydrogenases. Curr Issues Mol Biol 6:159–188PubMedGoogle Scholar
  68. Ward DE, Donnelly CJ, Mullendore ME, van der Oost J, de Vos WM, Crane EJ 3rd (2001) The NADH oxidase from Pyrococcus furiosus. Implications for the protection of anaerobic hyperthermophiles against oxidative stress. Eur J Biochem 268:5816–5823PubMedCrossRefGoogle Scholar
  69. Watrin L, Prieur D (1996) UV and ethyl methanesulfonate effects in hyperthermophilic archaea and isolation of auxtrophic mutants of Pyrococcus strains. Curr Microbiol 33:377–382PubMedCrossRefGoogle Scholar
  70. Weinberg MV, Jenney FE Jr, Cui X, Adams MWW (2004) Rubrerythrin from the hyperthermophilic archaeon Pyrococcus furiosus is a rubredoxin-dependent, iron-containing peroxidase. J Bacteriol 186:7888–7895PubMedCrossRefGoogle Scholar
  71. Whitehead K, Kish A, Pan M, Kaur A, King N, Hohmann L, DiRuggiero J, Baliga NS (2006) Stress management: using a systems approach to understand stress response to gamma radiation. Mol Syst Biol (in press)Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Ernest Williams
    • 1
  • Todd M. Lowe
    • 2
  • Jeffrey Savas
    • 2
  • Jocelyne DiRuggiero
    • 1
  1. 1.Department of Cell Biology and Molecular GeneticsUniversity of MarylandCollege ParkUSA
  2. 2.Department of Biomolecular Engineering, UCSC RNA CenterUniversity of California, Santa CruzSanta CruzUSA

Personalised recommendations