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Oxidative stress protection and the repair response to hydrogen peroxide in the hyperthermophilic archaeon Pyrococcus furiosus and in related species

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Abstract

Pyrococcus furiosus is a shallow marine, anaerobic archaeon that grows optimally at 100°C. Addition of H2O2 (0.5 mM) to a growing culture resulted in the cessation of growth with a 2-h lag before normal growth resumed. Whole genome transcriptional profiling revealed that the main response occurs within 30 min of peroxide addition, with the up-regulation of 62 open reading frames (ORFs), 36 of which are part of 10 potential operons. More than half of the up-regulated ORFs are of unknown function, while some others encode proteins that are involved potentially in sequestering iron and sulfide, in DNA repair and in generating NADPH. This response is thought to involve primarily damage repair rather than protection, since cultures exposed to sub-toxic levels of H2O2 were not more resistant to the subsequent addition of H2O2 (0.5–5.0 mM). Consequently, there is little if any induced protective response to peroxide. The organism maintains a constitutive protective mechanism involving high levels of oxidoreductase-type enzymes such as superoxide reductase, rubrerythrin, and alkyl hydroperoxide reductase. Related hyperthermophiles contain homologs of the proteins involved in the constitutive protective mechanism but these organisms were more sensitive to peroxide than P. furiosus and lack several of its peroxide-responsive ORFs.

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References

  • Almeida CC, Romao CV, Lindley PF, Teixeira M, Saraiva LM (2006) The role of the hybrid cluster protein in oxidative stress defense. J Biol Chem 281:32445–32450

    Article  CAS  PubMed  Google Scholar 

  • Almiron M, Link AJ, Furlong D, Kolter R (1992) A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev 6:2646–2654

    Article  CAS  PubMed  Google Scholar 

  • Atomi H, Fukui T, Kanai T, Morikawa M, Imanaka T (2004) Description of Thermococcus kodakaraensis sp. nov., a well studied hyperthermophilic archaeon previously reported as Pyrococcus sp. KOD1. Archaea 1:263–267

    Article  CAS  PubMed  Google Scholar 

  • Briolat V, Reysset G (2002) Identification of the Clostridium perfringens genes involved in the adaptive response to oxidative stress. J Bacteriol 184:2333–2343

    Article  CAS  PubMed  Google Scholar 

  • Ceci P, Cellai S, Falvo E, Rivetti C, Rossi GL, Chiancone E (2004) DNA condensation and self-aggregation of Escherichia coli Dps are coupled phenomena related to the properties of the N-terminus. Nucleic Acids Res 32:5935–5944

    Article  CAS  PubMed  Google Scholar 

  • Cohen GN, Barbe V, Flament D, Galperin M, Heilig R, Lecompte O, Poch O, Prieur D, Querellou J, Ripp R, Thierry JC, Van der Oost J, Weissenbach J, Zivanovic Y, Forterre P (2003) An integrated analysis of the genome of the hyperthermophilic archaeon Pyrococcus abyssi. Mol Microbiol 47:1495–1512

    Article  CAS  PubMed  Google Scholar 

  • Cypionka H (2000) Oxygen respiration by Desulfovibrio species. Annu Rev Microbiol 54:827–848

    Article  CAS  PubMed  Google Scholar 

  • Delphine J, Briolat V, Reysset G (2004) Oxidative stress response in Clostridium perfringens. Microbiology 150:1649–1659

    Article  CAS  Google Scholar 

  • Diaz PI, Slakeski N, Reynolds EC, Morona R, Rogers AH, Kolenbrander PE (2006) Role of oxyR in the oral anaerobe Porphyromonas gingivalis. J Bacteriol 188:2454–2462

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Emerson JE, Stabler RA, Wren BW, Fairweather NF (2008) Microarray analysis of the transcriptional responses of Clostridium difficile to environmental and antibiotic stress. J Med Microbiol 57:757–764

    Article  CAS  PubMed  Google Scholar 

  • Farr SB, Kogoma T (1991) Oxidative stress responses in Escherichia coli and Salmonella typhimurium. Microbiol Rev 55:561–585

    CAS  PubMed  Google Scholar 

  • Fournier M, Aubert C, Dermoun Z, Durand MC, Moinier D, Dolla A (2006) Response of the anaerobe Desulfovibrio vulgaris Hildenborough to oxidative conditions: proteome and transcript analysis. Biochimie 88:85–94

    Article  CAS  PubMed  Google Scholar 

  • Fridovich I (1978) The biology of oxygen radicals. Science 201:875–880

    Article  CAS  PubMed  Google Scholar 

  • Fukui T, Atomi H, Kanai T, Matsumi R, Fujiwara S, Imanaka T (2005) Complete genome sequence of the hyperthermophilic archaeon Thermococcus kodakaraensis KOD1 and comparison with Pyrococcus genomes. Genome Res 15:352–363

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez JM, Masuchi Y, Robb FT, Ammerman JW, Maeder DL, Yanagibayashi M, Tamaoka J, Kato C (1998) Pyrococcus horikoshii sp. nov., a hyperthermophilic archaeon isolated from a hydrothermal vent at the Okinawa Trough. Extremophiles 2:123–130

    Article  CAS  PubMed  Google Scholar 

  • Grunden AM, Jenney FE Jr, Ma K, Ji M, Weinberg MV, Adams MW (2005) In vitro reconstitution of an NADPH-dependent superoxide reduction pathway from Pyrococcus furiosus. Appl Environ Microbiol 71:1522–1530

    Article  CAS  PubMed  Google Scholar 

  • Hamilton-Brehm SD, Schut GJ, Adams MW (2005) Metabolic and evolutionary relationships among Pyrococcus species: genetic exchange within a hydrothermal vent environment. J Bacteriol 187:7492–7499

    Article  CAS  PubMed  Google Scholar 

  • Heidelberg JF, Seshadri R, Haveman SA, Hemme CL, Paulsen IT, Kolonay JF, Eisen JA, Ward N, Methe B, Brinkac LM, Daugherty SC, Deboy RT, Dodson RJ, Durkin AS, Madupu R, Nelson WC, Sullivan SA, Fouts D, Haft DH, Selengut J, Peterson JD, Davidsen TM, Zafar N, Zhou L, Radune D, Dimitrov G, Hance M, Tran K, Khouri H, Gill J, Utterback TR, Feldblyum TV, Wall JD, Voordouw G, Fraser CM (2004) The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat Biotechnol 22:554–559

    Article  CAS  PubMed  Google Scholar 

  • Helmann JD, Wu MF, Gaballa A, Kobel PA, Morshedi MM, Fawcett P, Paddon C (2003) The global transcriptional response of Bacillus subtilis to peroxide stress is coordinated by three transcription factors. J Bacteriol 185:243–253

    Article  CAS  PubMed  Google Scholar 

  • Holden JF, Poole FL II, Tollaksen SL, Giometti CS, Lim H, Yates JR 3rd, Adams MW (2001) Identification of membrane proteins in the hyperthermophilic archaeon Pyrococcus furiosus using proteomics and prediction programs. Comp Funct Genomics 2:275–288

    Article  CAS  PubMed  Google Scholar 

  • Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  • Imlay JA (2003) Pathways of oxidative damage. Annu Rev Microbiol 57:395–418

    Article  CAS  PubMed  Google Scholar 

  • Imlay JA (2008a) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77:755–776

    Article  CAS  PubMed  Google Scholar 

  • Imlay JA (2008b) How obligatory is anaerobiosis? Mol Microbiol 68:801–804

    Article  CAS  PubMed  Google Scholar 

  • Jenney FE Jr, Verhagen MF, Cui X, Adams MW (1999) Anaerobic microbes: oxygen detoxification without superoxide dismutase. Science 286:306–309

    Article  CAS  PubMed  Google Scholar 

  • 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 136:541–547

    Article  CAS  PubMed  Google Scholar 

  • Kawarabayasi Y, Sawada M, Horikawa H, Haikawa Y, Hino Y, Yamamoto S, Sekine M, Baba S, Kosugi H, Hosoyama A, Nagai Y, Sakai M, Ogura K, Otsuka R, Nakazawa H, Takamiya M, Ohfuku Y, Funahashi T, Tanaka T, Kudoh Y, Yamazaki J, Kushida N, Oguchi A, Aoki K, Kikuchi H (1998) Complete sequence and gene organization of the genome of a hyper-thermophilic archaebacterium, Pyrococcus horikoshii OT3 (supplement). DNA Res 5:147–155

    Article  CAS  PubMed  Google Scholar 

  • Kengen SW, Luesink EJ, Stams AJ, Zehnder AJ (1993) Purification and characterization of an extremely thermostable beta-glucosidase from the hyperthermophilic archaeon Pyrococcus furiosus. Eur J Biochem 213:305–312

    Article  CAS  PubMed  Google Scholar 

  • Kieber RJ, Cooper WJ, Willey JD, Brooks Avery Jr G (2001) Hydrogen peroxide at the Bermuda Atlantic Time Series Station. Part 1: temporal variability of atmospheric hydrogen peroxide and its influence on seawater concentrations. J Atmosph Chem 39:1–13

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kurtz DM Jr (2006) Avoiding high-valent iron intermediates: superoxide reductase and rubrerythrin. J Inorg Biochem 100:679–693

    Article  CAS  PubMed  Google Scholar 

  • Lesser MP (2006) Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68:253–278

    Article  CAS  PubMed  Google Scholar 

  • Ma K, Adams MW (2001) Hydrogenases I and II from Pyrococcus furiosus. Methods Enzymol 331:208–216

    Article  CAS  PubMed  Google Scholar 

  • Morikawa M, Izawa Y, Rashid N, Hoaki T, Imanaka T (1994) Purification and characterization of a thermostable thiol protease from a newly isolated hyperthermophilic Pyrococcus sp. Appl Environ Microbiol 60:4559–4566

    CAS  PubMed  Google Scholar 

  • Mukhopadhyay A, Redding AM, Joachimiak MP, Arkin AP, Borglin SE, Dehal PS, Chakraborty R, Geller JT, Hazen TC, He Q, Joyner DC, Martin VJ, Wall JD, Yang ZK, Zhou J, Keasling JD (2007) Cell-wide responses to low-oxygen exposure in Desulfovibrio vulgaris Hildenborough. J Bacteriol 189:5996–6010

    Article  CAS  PubMed  Google Scholar 

  • Nakayama K (1994) Rapid viability loss on exposure to air in a superoxide dismutase-deficient mutant of Porphyromonas gingivalis. J Bacteriol 176:1939–1943

    CAS  PubMed  Google Scholar 

  • Omsland A, Miranda KM, Friedman RL, Boitano S (2008) Bordetella bronchiseptica responses to physiological reactive nitrogen and oxygen stresses. FEMS Microbiol Lett 284:92–101

    Article  CAS  PubMed  Google Scholar 

  • Oremland RS (1988) Biogeochemistry of methanogenic bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 641–706

    Google Scholar 

  • Palma M, DeLuca D, Worgall S, Quadri LE (2004) Transcriptome analysis of the response of Pseudomonas aeruginosa to hydrogen peroxide. J Bacteriol 186:248–252

    Article  CAS  PubMed  Google Scholar 

  • Pereira PM, He Q, Xavier AV, Zhou J, Pereira IA, Louro RO (2008) Transcriptional response of Desulfovibrio vulgaris Hildenborough to oxidative stress mimicking environmental conditions. Arch Microbiol 189:451–461

    Article  CAS  PubMed  Google Scholar 

  • Poole FL II, Gerwe BA, Hopkins RC, Schut GJ, Weinberg MV, Jenney FE Jr, Adams MW (2005) Defining genes in the genome of the hyperthermophilic archaeon Pyrococcus furiosus: implications for all microbial genomes. J Bacteriol 187:7325–7332

    Article  CAS  PubMed  Google Scholar 

  • Ramsay B, Wiedenheft B, Allen M, Gauss GH, Lawrence CM, Young M, Douglas T (2006) Dps-like protein from the hyperthermophilic archaeon Pyrococcus furiosus. J Inorg Biochem 100:1061–1068

    Article  CAS  PubMed  Google Scholar 

  • Rocha ER, Selby T, Coleman JP, Smith CJ (1996) Oxidative stress response in an anaerobe, Bacteroides fragilis: a role for catalase in protection against hydrogen peroxide. J Bacteriol 178:6895–6903

    CAS  PubMed  Google Scholar 

  • Sapra R, Verhagen MF, Adams MW (2000) Purification and characterization of a membrane-bound hydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 182:3423–3428

    Article  CAS  PubMed  Google Scholar 

  • Schroder E, Ponting CP (1998) Evidence that peroxiredoxins are novel members of the thioredoxin fold superfamily. Protein Sci 7:2465–2468

    Article  CAS  PubMed  Google Scholar 

  • Schut GJ, Zhou J, Adams MW (2001) DNA microarray analysis of the hyperthermophilic archaeon Pyrococcus furiosus: evidence for a new type of sulfur-reducing enzyme complex. J Bacteriol 183:7027–7036

    Article  CAS  PubMed  Google Scholar 

  • Schut GJ, Brehm SD, Datta S, Adams MW (2003) Whole-genome DNA microarray analysis of a hyperthermophile and an archaeon: Pyrococcus furiosus grown on carbohydrates or peptides. J Bacteriol 185:3935–3947

    Article  CAS  PubMed  Google Scholar 

  • Schut GJ, Bridger SL, Adams MW (2007) Insights into the metabolism of elemental sulfur by the hyperthermophilic archaeon Pyrococcus furiosus: characterization of a coenzyme A-dependent NAD(P)H sulfur oxidoreductase. J Bacteriol 189:4431–4441

    Article  CAS  PubMed  Google Scholar 

  • Smet E, Lens P, Van Langenhove H (1998) Treatment of waste gases contaminated with odorous sulfur compounds. Crit Rev Environ Sci Technol 28:89–117

    Article  CAS  Google Scholar 

  • Stetter KO (1982) Ultrathin mycelia-forming organisms from submarine volcanic areas having an optimum growth temperature of 105°C. Nature 300:258–259

    Article  Google Scholar 

  • Stohl EA, Criss AK, Seifert HS (2005) The transcriptome response of Neisseria gonorrhoeae to hydrogen peroxide reveals genes with previously uncharacterized roles in oxidative damage protection. Mol Microbiol 58:520–532

    Article  CAS  PubMed  Google Scholar 

  • Storz G, Imlay JA (1999) Oxidative stress. Curr Opin Microbiol 2:188–194

    Article  CAS  PubMed  Google Scholar 

  • Sund CJ, Rocha ER, Tzianabos AO, Wells WG, Gee JM, Reott MA, O’Rourke DP, Smith CJ (2008) The Bacteroides fragilis transcriptome response to oxygen and H2O2: the role of OxyR and its effect on survival and virulence. Mol Microbiol 67:129–142

    Article  CAS  PubMed  Google Scholar 

  • Tapley DW, Buettner GR, Shick JM (1999) Free radicals and chemiluminescence as products of the spontaneous oxidation of sulfide in seawater, and their biological implications. Biol Bull 196:52–56

    Article  CAS  Google Scholar 

  • Tatur J, Hagedoorn PL, Overeijnder ML, Hagen WR (2006) A highly thermostable ferritin from the hyperthermophilic archaeal anaerobe Pyrococcus furiosus. Extremophiles 10:139–148

    Article  CAS  PubMed  Google Scholar 

  • Tran TT, Dam P, Su Z, Poole FL II, Adams MW, Zhou GT, Xu Y (2007) Operon prediction in Pyrococcus furiosus. Nucleic Acids Res 35:11–20

    Article  CAS  PubMed  Google Scholar 

  • van der Oost J, Voorhorst WG, Kengen SW, Geerling AC, Wittenhorst V, Gueguen Y, de Vos WM (2001) Genetic and biochemical characterization of a short-chain alcohol dehydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus. Eur J Biochem 268:3062–3068

    Article  PubMed  Google Scholar 

  • Weinberg MV, Jenney FE Jr, Cui X, Adams MW (2004) Rubrerythrin from the hyperthermophilic archaeon Pyrococcus furiosus is a rubredoxin-dependent, iron-containing peroxidase. J Bacteriol 186:7888–7895

    Article  CAS  PubMed  Google Scholar 

  • Weinberg MV, Schut GJ, Brehm S, Datta S, Adams MW (2005) Cold shock of a hyperthermophilic archaeon: Pyrococcus furiosus exhibits multiple responses to a suboptimal growth temperature with a key role for membrane-bound glycoproteins. J Bacteriol 187:336–348

    Article  CAS  PubMed  Google Scholar 

  • Wiedenheft B, Mosolf J, Willits D, Yeager M, Dryden KA, Young M, Douglas T (2005) An archaeal antioxidant: characterization of a Dps-like protein from Sulfolobus solfataricus. Proc Natl Acad Sci USA 102:10551–10556

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Zhang W, Culley DE, Hogan M, Vitiritti L, Brockman FJ (2006) Oxidative stress and heat-shock responses in Desulfovibrio vulgaris by genome-wide transcriptomic analysis. Antonie Van Leeuwenhoek 90:41–55

    Article  CAS  PubMed  Google Scholar 

  • Zhao G, Bou-Abdallah F, Arosio P, Levi S, Janus-Chandler C, Chasteen ND (2003) Multiple pathways for mineral core formation in mammalian apoferritin. The role of hydrogen peroxide. Biochemistry 42:3142–3150

    Article  CAS  PubMed  Google Scholar 

  • Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, Storz G (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183:4562–4570

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. Haruyuki Atomi for the kind gift of Thermococcus kodakaraensis KOD1 and Scott D. Hamilton-Brehm, Angeli Lal Menon, Sonya Clarkson and Farris Poole for many helpful discussions. This research was supported by a postdoctoral fellowship (to KRS) from the Norwegian Research Council and grants (to MWA) from the National Institutes of Health (GM 60329) and the Department of Energy (FG05-95ER20175 and FG02-08ER64690).

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  1. Kari R. Strand

    Present address: Department of Molecular Biosciences, University of Oslo, Oslo, Norway

  2. Francis E. Jenney Jr.

    Present address: Department of Basic Sciences, Georgia Campus Philadelphia College of Osteopathic Medicine, Suwanee, GA, 30024, USA

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  1. Department of Biochemistry and Molecular Biology, University of Georgia, Life Sciences Bldg., Athens, GA, 30602-7229, USA

    Kari R. Strand, Chengjun Sun, Ting Li, Francis E. Jenney Jr., Gerrit J. Schut & Michael W. W. Adams

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Strand, K.R., Sun, C., Li, T. et al. Oxidative stress protection and the repair response to hydrogen peroxide in the hyperthermophilic archaeon Pyrococcus furiosus and in related species. Arch Microbiol 192, 447–459 (2010). https://doi.org/10.1007/s00203-010-0570-z

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