Differential response of to varying levels and duration of hydrogen peroxide-induced oxidative stress Free

Abstract

, an anaerobic oral pathogen implicated in adult periodontitis, can exist in an environment of oxidative stress. To evaluate its adaptation to this environment, we have assessed the response of W83 to varying levels and durations of hydrogen peroxide (HO)-induced stress. When was initially exposed to a subinhibitory concentration of HO (0.1 mM), an adaptive response to higher concentrations could be induced. Transcriptome analysis demonstrated that oxidative stress can modulate several functional classes of genes depending on the severity and duration of the exposure. A 10 min exposure to HO revealed increased expression of genes involved in DNA damage and repair, while after 15 min, genes involved in protein fate, protein folding and stabilization were upregulated. Approximately 9 and 2.8 % of the genome displayed altered expression in response to HO exposure at 10 and 15 min, respectively. Substantially more genes were upregulated (109 at 10 min; 47 at 15 min) than downregulated (76 at 10 min; 11 at 15 min) by twofold or higher in response to HO exposure. The majority of these modulated genes were hypothetical or of unknown function. One of those genes () with DNA-binding properties that was upregulated during prolonged oxidative stress was inactivated by allelic exchange mutagenesis. The isogenic mutant FLL363 ( : : ) showed increased sensitivity to HO compared with the parent strain. Collectively, our data indicate the adaptive ability of to oxidative stress and further underscore the complex nature of its resistance strategy under those conditions.

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2012-10-01
2024-03-29
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References

  1. Abaibou H., Chen Z., Olango G. J., Liu Y., Edwards J., Fletcher H. M. ( 2001). vimA gene downstream of recA is involved in virulence modulation in Porphyromonas gingivalis W83. Infect Immun 69:325–335 [View Article][PubMed]
    [Google Scholar]
  2. Araki M., Hiratsuka K., Kiyama-Kishikawa M., Abiko Y. ( 2004). Monitoring of dnaK gene expression in Porphyromonas gingivalis by oxygen stress using DNA microarray. J Oral Sci 46:93–100 [View Article][PubMed]
    [Google Scholar]
  3. Barnard J. P., Stinson M. W. ( 1996). The alpha-hemolysin of Streptococcus gordonii is hydrogen peroxide. Infect Immun 64:3853–3857[PubMed]
    [Google Scholar]
  4. Barnard J. P., Stinson M. W. ( 1999). Influence of environmental conditions on hydrogen peroxide formation by Streptococcus gordonii . Infect Immun 67:6558–6564[PubMed]
    [Google Scholar]
  5. Beaman L., Beaman B. L. ( 1984). The role of oxygen and its derivatives in microbial pathogenesis and host defense. Annu Rev Microbiol 38:27–48 [View Article][PubMed]
    [Google Scholar]
  6. Berndt C., Lillig C. H., Holmgren A. ( 2008). Thioredoxins and glutaredoxins as facilitators of protein folding. Biochim Biophys Acta 1783:641–650 [View Article][PubMed]
    [Google Scholar]
  7. Bitoun J. P., Wu G., Ding H. ( 2008). Escherichia coli FtnA acts as an iron buffer for re-assembly of iron-sulfur clusters in response to hydrogen peroxide stress. Biometals 21:693–703 [View Article][PubMed]
    [Google Scholar]
  8. Brioukhanov A. L., Netrusov A. I. ( 2004). Catalase and superoxide dismutase: distribution, properties, and physiological role in cells of strict anaerobes. Biochemistry (Mosc) 69:949–962 [View Article][PubMed]
    [Google Scholar]
  9. Brochu V., Grenier D., Nakayama K., Mayrand D. ( 2001). Acquisition of iron from human transferrin by Porphyromonas gingivalis: a role for Arg- and Lys-gingipain activities. Oral Microbiol Immunol 16:79–87 [View Article][PubMed]
    [Google Scholar]
  10. Cadet J., Bourdat A. G., D’Ham C., Duarte V., Gasparutto D., Romieu A., Ravanat J. L. ( 2000). Oxidative base damage to DNA: specificity of base excision repair enzymes. Mutat Res 462:121–128 [View Article][PubMed]
    [Google Scholar]
  11. Canakçi C. F., Ciçek Y., Canakçi V. ( 2005). Reactive oxygen species and human inflammatory periodontal diseases. Biochemistry (Mosc) 70:619–628 [View Article][PubMed]
    [Google Scholar]
  12. Champagne C. M., Buchanan W., Reddy M. S., Preisser J. S., Beck J. D., Offenbacher S. ( 2003). Potential for gingival crevice fluid measures as predictors of risk for periodontal diseases. Periodontol 2000 31:167–180 [View Article][PubMed]
    [Google Scholar]
  13. Chang W., Small D. A., Toghrol F., Bentley W. E. ( 2005). Microarray analysis of Pseudomonas aeruginosa reveals induction of pyocin genes in response to hydrogen peroxide. BMC Genomics 6:115 [View Article][PubMed]
    [Google Scholar]
  14. Chapple I. L. ( 1996). Role of free radicals and antioxidants in the pathogenesis of the inflammatory periodontal diseases. Clin Mol Pathol 49:M247–M255 [View Article][PubMed]
    [Google Scholar]
  15. Chiancone E., Ceci P., Ilari A., Ribacchi F., Stefanini S. ( 2004). Iron and proteins for iron storage and detoxification. Biometals 17:197–202 [View Article][PubMed]
    [Google Scholar]
  16. Conrads G., Herrler A., Moonen I., Lampert F., Schnitzler N. ( 1999). Flow cytometry to monitor phagocytosis and oxidative burst of anaerobic periodontopathogenic bacteria by human polymorphonuclear leukocytes. J Periodontal Res 34:136–144 [View Article][PubMed]
    [Google Scholar]
  17. Dashper S. G., Cross K. J., Slakeski N., Lissel P., Aulakh P., Moore C., Reynolds E. C. ( 2004). Hemoglobin hydrolysis and heme acquisition by Porphyromonas gingivalis . Oral Microbiol Immunol 19:50–56 [View Article][PubMed]
    [Google Scholar]
  18. Dashper S. G., Butler C. A., Lissel J. P., Paolini R. A., Hoffmann B., Veith P. D., O’Brien-Simpson N. M., Snelgrove S. L., Tsiros J. T., Reynolds E. C. ( 2005). A novel Porphyromonas gingivalis FeoB plays a role in manganese accumulation. J Biol Chem 280:28095–28102 [View Article][PubMed]
    [Google Scholar]
  19. Diaz P. I., Rogers A. H. ( 2004). The effect of oxygen on the growth and physiology of Porphyromonas gingivalis . Oral Microbiol Immunol 19:88–94 [View Article][PubMed]
    [Google Scholar]
  20. Diaz P. I., Slakeski N., Reynolds E. C., Morona R., Rogers A. H., Kolenbrander P. E. ( 2006). Role of oxyR in the oral anaerobe Porphyromonas gingivalis . J Bacteriol 188:2454–2462 [View Article][PubMed]
    [Google Scholar]
  21. Dou Y., Osbourne D., McKenzie R., Fletcher H. M. ( 2010). Involvement of extracytoplasmic function sigma factors in virulence regulation in Porphyromonas gingivalis W83. FEMS Microbiol Lett 312:24–32 [View Article][PubMed]
    [Google Scholar]
  22. Emerson J. E., Stabler R. A., Wren B. W., Fairweather N. F. ( 2008). Microarray analysis of the transcriptional responses of Clostridium difficile to environmental and antibiotic stress. J Med Microbiol 57:757–764 [View Article][PubMed]
    [Google Scholar]
  23. Fletcher H. M., Schenkein H. A., Morgan R. M., Bailey K. A., Berry C. R., Macrina F. L. ( 1995). Virulence of a Porphyromonas gingivalis W83 mutant defective in the prtH gene. Infect Immun 63:1521–1528[PubMed]
    [Google Scholar]
  24. Forng R. Y., Champagne C., Simpson W., Genco C. A. ( 2000). Environmental cues and gene expression in Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans . Oral Dis 6:351–365 [View Article][PubMed]
    [Google Scholar]
  25. Gardner R. G., Russell J. B., Wilson D. B., Wang G. R., Shoemaker N. B. ( 1996). Use of a modified Bacteroides-Prevotella shuttle vector to transfer a reconstructed beta-1,4-d-endoglucanase gene into Bacteroides uniformis and Prevotella ruminicola B14. Appl Environ Microbiol 62:196–202[PubMed]
    [Google Scholar]
  26. Genco C. A., Dixon D. W. ( 2001). Emerging strategies in microbial haem capture. Mol Microbiol 39:1–11 [View Article][PubMed]
    [Google Scholar]
  27. Genevaux P., Georgopoulos C., Kelley W. L. ( 2007). The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions. Mol Microbiol 66:840–857 [View Article][PubMed]
    [Google Scholar]
  28. Grifantini R., Frigimelica E., Delany I., Bartolini E., Giovinazzi S., Balloni S., Agarwal S., Galli G., Genco C., Grandi G. ( 2004). Characterization of a novel Neisseria meningitidis Fur and iron-regulated operon required for protection from oxidative stress: utility of DNA microarray in the assignment of the biological role of hypothetical genes. Mol Microbiol 54:962–979 [View Article][PubMed]
    [Google Scholar]
  29. He J., Miyazaki H., Anaya C., Yu F., Yeudall W. A., Lewis J. P. ( 2006). Role of Porphyromonas gingivalis FeoB2 in metal uptake and oxidative stress protection. Infect Immun 74:4214–4223 [View Article][PubMed]
    [Google Scholar]
  30. Henry L. G., McKenzie R. M., Robles A., Fletcher H. M. ( 2012). Oxidative stress resistance in Porphyromonas gingivalis . Future Microbiol 7:497–512 [View Article][PubMed]
    [Google Scholar]
  31. Johnson N. A., Liu Y., Fletcher H. M. ( 2004a). Alkyl hydroperoxide peroxidase subunit C (ahpC) protects against organic peroxides but does not affect the virulence of Porphyromonas gingivalis W83. Oral Microbiol Immunol 19:233–239 [View Article][PubMed]
    [Google Scholar]
  32. Johnson N. A., McKenzie R., McLean L., Sowers L. C., Fletcher H. M. ( 2004b). 8-oxo-7,8-dihydroguanine is removed by a nucleotide excision repair-like mechanism in Porphyromonas gingivalis W83. J Bacteriol 186:7697–7703 [View Article][PubMed]
    [Google Scholar]
  33. Johnson L. S., Eddy S. R., Portugaly E. ( 2010). Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics 11:431 [View Article][PubMed]
    [Google Scholar]
  34. Johnson N. A., McKenzie R. M., Fletcher H. M. ( 2011). The bcp gene in the bcp-recA-vimA-vimE-vimF operon is important in oxidative stress resistance in Porphyromonas gingivalis W83. Mol Oral Microbiol 26:62–77 [View Article][PubMed]
    [Google Scholar]
  35. Koháryová M., Kolárová M. ( 2008). Oxidative stress and thioredoxin system. Gen Physiol Biophys 27:71–84[PubMed]
    [Google Scholar]
  36. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A. & other authors ( 2007). clustal w and clustal_x version 2.0. Bioinformatics 23:2947–2948 [View Article][PubMed]
    [Google Scholar]
  37. Lewis J. P., Dawson J. A., Hannis J. C., Muddiman D., Macrina F. L. ( 1999). Hemoglobinase activity of the lysine gingipain protease (Kgp) of Porphyromonas gingivalis W83. J Bacteriol 181:4905–4913[PubMed]
    [Google Scholar]
  38. Lewis J. P., Iyer D., Anaya-Bergman C. ( 2009). Adaptation of Porphyromonas gingivalis to microaerophilic conditions involves increased consumption of formate and reduced utilization of lactate. Microbiology 155:3758–3774 [View Article][PubMed]
    [Google Scholar]
  39. Lushchak V. I. ( 2001). Oxidative stress and mechanisms of protection against it in bacteria. Biochemistry (Mosc) 66:476–489 [View Article][PubMed]
    [Google Scholar]
  40. Marcotte E. M., Pellegrini M., Ng H. L., Rice D. W., Yeates T. O., Eisenberg D. ( 1999). Detecting protein function and protein-protein interactions from genome sequences. Science 285:751–753 [View Article][PubMed]
    [Google Scholar]
  41. Marquis R. E. ( 1995). Oxygen metabolism, oxidative stress and acid-base physiology of dental plaque biofilms. J Ind Microbiol 15:198–207 [View Article][PubMed]
    [Google Scholar]
  42. Martin J. A., Page R. C., Kaye E. K., Hamed M. T., Loeb C. F. ( 2009). Periodontitis severity plus risk as a tooth loss predictor. J Periodontol 80:202–209 [View Article][PubMed]
    [Google Scholar]
  43. Mereghetti L., Sitkiewicz I., Green N. M., Musser J. M. ( 2008). Extensive adaptive changes occur in the transcriptome of Streptococcus agalactiae (group B streptococcus) in response to incubation with human blood. PLoS ONE 3:e3143 [View Article][PubMed]
    [Google Scholar]
  44. Meuric V., Gracieux P., Tamanai-Shacoori Z., Perez-Chaparro J., Bonnaure-Mallet M. ( 2008). Expression patterns of genes induced by oxidative stress in Porphyromonas gingivalis . Oral Microbiol Immunol 23:308–314 [View Article][PubMed]
    [Google Scholar]
  45. Nelson K. E., Fleischmann R. D., DeBoy R. T., Paulsen I. T., Fouts D. E., Eisen J. A., Daugherty S. C., Dodson R. J., Durkin A. S. & other authors ( 2003). Complete genome sequence of the oral pathogenic bacterium Porphyromonas gingivalis strain W83. J Bacteriol 185:5591–5601 [View Article][PubMed]
    [Google Scholar]
  46. Ohara N., Kikuchi Y., Shoji M., Naito M., Nakayama K. ( 2006). Superoxide dismutase-encoding gene of the obligate anaerobe Porphyromonas gingivalis is regulated by the redox-sensing transcription activator OxyR. Microbiology 152:955–966 [View Article][PubMed]
    [Google Scholar]
  47. Okamoto K., Nakayama K., Kadowaki T., Abe N., Ratnayake D. B., Yamamoto K. ( 1998). Involvement of a lysine-specific cysteine proteinase in hemoglobin adsorption and heme accumulation by Porphyromonas gingivalis . J Biol Chem 273:21225–21231 [View Article][PubMed]
    [Google Scholar]
  48. Pomposiello P. J., Demple B. ( 2002). Global adjustment of microbial physiology during free radical stress. Adv Microb Physiol 46:319–341 [View Article][PubMed]
    [Google Scholar]
  49. Potempa J., Sroka A., Imamura T., Travis J. ( 2003). Gingipains, the major cysteine proteinases and virulence factors of Porphyromonas gingivalis: structure, function and assembly of multidomain protein complexes. Curr Protein Pept Sci 4:397–407 [View Article][PubMed]
    [Google Scholar]
  50. Robles A. G., Reid K., Roy F., Fletcher H. M. ( 2011). Porphyromonas gingivalis mutY is involved in the repair of oxidative stress-induced DNA mispairing. Mol Oral Microbiol 26:175–186 [View Article][PubMed]
    [Google Scholar]
  51. Ryan C. S., Kleinberg I. ( 1995). Bacteria in human mouths involved in the production and utilization of hydrogen peroxide. Arch Oral Biol 40:753–763 [View Article][PubMed]
    [Google Scholar]
  52. Salunkhe P., Töpfer T., Buer J., Tümmler B. ( 2005). Genome-wide transcriptional profiling of the steady-state response of Pseudomonas aeruginosa to hydrogen peroxide. J Bacteriol 187:2565–2572 [View Article][PubMed]
    [Google Scholar]
  53. Shelburne C. E., Shelburne P. S., Dhople V. M., Sweier D. G., Giannobile W. V., Kinney J. S., Coulter W. A., Mullally B. H., Lopatin D. E. ( 2008). Serum antibodies to Porphyromonas gingivalis chaperone HtpG predict health in periodontitis susceptible patients. PLoS ONE 3:e1984 [View Article][PubMed]
    [Google Scholar]
  54. Shevchuk N. A., Bryksin A. V., Nusinovich Y. A., Cabello F. C., Sutherland M., Ladisch S. ( 2004). Construction of long DNA molecules using long PCR-based fusion of several fragments simultaneously. Nucleic Acids Res 32:e19 [View Article][PubMed]
    [Google Scholar]
  55. Shi Y., Ratnayake D. B., Okamoto K., Abe N., Yamamoto K., Nakayama K. ( 1999). Genetic analyses of proteolysis, hemoglobin binding, and hemagglutination of Porphyromonas gingivalis. Construction of mutants with a combination of rgpA, rgpB, kgp, and hagA . J Biol Chem 274:17955–17960 [View Article][PubMed]
    [Google Scholar]
  56. Singh V. K., Utaida S., Jackson L. S., Jayaswal R. K., Wilkinson B. J., Chamberlain N. R. ( 2007). Role for dnaK locus in tolerance of multiple stresses in Staphylococcus aureus . Microbiology 153:3162–3173 [View Article][PubMed]
    [Google Scholar]
  57. Smalley J. W., Silver J., Marsh P. J., Birss A. J. ( 1998). The periodontopathogen Porphyromonas gingivalis binds iron protoporphyrin IX in the mu-oxo dimeric form: an oxidative buffer and possible pathogenic mechanism. Biochem J 331:681–685[PubMed]
    [Google Scholar]
  58. Smalley J. W., Birss A. J., Silver J. ( 2000). The periodontal pathogen Porphyromonas gingivalis harnesses the chemistry of the mu-oxo bishaem of iron protoporphyrin IX to protect against hydrogen peroxide. FEMS Microbiol Lett 183:159–164[PubMed]
    [Google Scholar]
  59. Smalley J. W., Birss A. J., Szmigielski B., Potempa J. ( 2006). The HA2 haemagglutinin domain of the lysine-specific gingipain (Kgp) of Porphyromonas gingivalis promotes micro-oxo bishaem formation from monomeric iron(III) protoporphyrin IX. Microbiology 152:1839–1845 [View Article][PubMed]
    [Google Scholar]
  60. Stintzi A. ( 2003). Gene expression profile of Campylobacter jejuni in response to growth temperature variation. J Bacteriol 185:2009–2016 [View Article][PubMed]
    [Google Scholar]
  61. Sund C. J., Rocha E. R., Tzianabos A. O., Wells W. G., Gee J. M., Reott M. A., O’Rourke D. P., Smith C. J. ( 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 [View Article][PubMed]
    [Google Scholar]
  62. Sztukowska M., Bugno M., Potempa J., Travis J., Kurtz D. M. Jr ( 2002). Role of rubrerythrin in the oxidative stress response of Porphyromonas gingivalis . Mol Microbiol 44:479–488 [View Article][PubMed]
    [Google Scholar]
  63. Ueshima J., Shoji M., Ratnayake D. B., Abe K., Yoshida S., Yamamoto K., Nakayama K. ( 2003). Purification, gene cloning, gene expression, and mutants of Dps from the obligate anaerobe Porphyromonas gingivalis . Infect Immun 71:1170–1178 [View Article][PubMed]
    [Google Scholar]
  64. Visick J. E., Clarke S. ( 1995). Repair, refold, recycle: how bacteria can deal with spontaneous and environmental damage to proteins. Mol Microbiol 16:835–845 [View Article][PubMed]
    [Google Scholar]
  65. Wettenhall J. M., Smyth G. K. ( 2004). limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 20:3705–3706 [View Article][PubMed]
    [Google Scholar]
  66. Wu H. J., Seib K. L., Srikhanta Y. N., Kidd S. P., Edwards J. L., Maguire T. L., Grimmond S. M., Apicella M. A., McEwan A. G., Jennings M. P. ( 2006). PerR controls Mn-dependent resistance to oxidative stress in Neisseria gonorrhoeae . Mol Microbiol 60:401–416 [View Article][PubMed]
    [Google Scholar]
  67. Yuan L., Rodrigues P. H., Bélanger M., Dunn W. Jr, Progulske-Fox A. ( 2007). The Porphyromonas gingivalis clpB gene is involved in cellular invasion in vitro and virulence in vivo . FEMS Immunol Med Microbiol 51:388–398 [View Article][PubMed]
    [Google Scholar]
  68. Yuan L., Rodrigues P. H., Bélanger M., Dunn W. A. Jr, Progulske-Fox A. ( 2008). Porphyromonas gingivalis htrA is involved in cellular invasion and in vivo survival. Microbiology 154:1161–1169 [View Article][PubMed]
    [Google Scholar]
  69. Zheng M., Wang X., Templeton L. J., Smulski D. R., LaRossa R. A., Storz G. ( 2001). DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183:4562–4570 [View Article][PubMed]
    [Google Scholar]
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