1887

Abstract

resides in the oxygen-rich environment of the upper respiratory tract, and therefore the ability to survive in the presence of oxygen is an important aspect of its survival. To investigate how adapts to oxygen, we determined the global gene expression profile of the micro-organism in aerobiosis and anaerobiosis. It was found that exposure to aerobiosis elevated the expression of 54 genes, while the expression of 15 genes was downregulated. Notably there were significant changes in putative genome plasticity and hypothetical genes. In addition, increased expression of , a putative transcriptional regulator, was detected. To test the role of Rgg in the pneumococcal oxidative stress response, an isogenic mutant was constructed. It was found that the mutant was sensitive to oxygen and paraquat, but not to HO. In addition, the absence of Rgg strongly reduced the biofilm-forming ability of an unencapsulated pneumococcus. Virulence studies showed that the median survival time of mice infected intranasally with the mutant was significantly longer than that of the wild-type-infected group, and the animals infected with the mutant developed septicaemia later than those infected intranasally with the wild-type.

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2009-12-01
2024-04-19
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References

  1. Abranches J., Candella M. M., Wen Z. T., Baker H. V., Burne R. A. 2006; Different roles of EIIABMan and EIIGlc in regulation of energy metabolism, biofilm development, and competence in Streptococcus mutans . J Bacteriol 188:3748–3756
    [Google Scholar]
  2. Alloing G., Granadel C., Morrison D. A., Claverys J. P. 1996; Competence pheromone, oligopeptide permease, and induction of competence in Streptococcus pneumoniae . Mol Microbiol 21:471–478
    [Google Scholar]
  3. Amster-Choder O. 2005; The bgl sensory system: a transmembrane signaling pathway controlling transcriptional antitermination. Curr Opin Microbiol 8:127–134
    [Google Scholar]
  4. Amster-Choder O., Wright A. 1997; BglG, the response regulator of the Escherichia coli bgl operon, is phosphorylated on a histidine residue. J Bacteriol 179:5621–5624
    [Google Scholar]
  5. Atack J. M., Harvey P., Jones M. A., Kelly D. J. 2008; The Campylobacter jejuni thiol peroxidases Tpx and Bcp both contribute to aerotolerance and peroxide-mediated stress resistance but have distinct substrate specificities. J Bacteriol 190:5279–5290
    [Google Scholar]
  6. Auzat I., Chapuy-Regaud S., Le Bras G., Dos Santos D., Ogunniyi A. D., Le Thomas I., Garel J. R., Paton J. C., Trombe M. C. 1999; The NADH oxidase of Streptococcus pneumoniae: its involvement in competence and virulence. Mol Microbiol 34:1018–1028
    [Google Scholar]
  7. Cha M. K., Kim W. C., Lim C. J., Kim K., Kim I. H. 2004; Escherichia coli periplasmic thiol peroxidase acts as lipid hydroperoxide peroxidase and the principal antioxidative function during anaerobic growth. J Biol Chem 279:8769–8778
    [Google Scholar]
  8. 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
    [Google Scholar]
  9. Chang W., Small D. A., Toghrol F., Bentley W. E. 2006; Global transcriptome analysis of Staphylococcus aureus response to hydrogen peroxide. J Bacteriol 188:1648–1659
    [Google Scholar]
  10. Chaussee M. S., Somerville G. A., Reitzer L., Musser J. M. 2003; Rgg coordinates virulence factor synthesis and metabolism in Streptococcus pyogenes . J Bacteriol 185:6016–6024
    [Google Scholar]
  11. Chaussee M. A., Callegari E. A., Chaussee M. S. 2004; Rgg regulates growth phase-dependent expression of proteins associated with secondary metabolism and stress in Streptococcus pyogenes . J Bacteriol 186:7091–7099
    [Google Scholar]
  12. Cianciotto N. P. 2001; Pathogenicity of Legionella pneumophila . Int J Med Microbiol 291:331–343
    [Google Scholar]
  13. Dagkessamanskaia A., Moscoso M., Henard V., Guiral S., Overweg K., Reuter M., Martin B., Wells J., Claverys J. P. 2004; Interconnection of competence, stress and CiaR regulons in Streptococcus pneumoniae: competence triggers stationary phase autolysis of ciaR mutant cells. Mol Microbiol 51:1071–1086
    [Google Scholar]
  14. Dmitriev A. V., McDowell E. J., Chaussee M. S. 2008; Inter- and intraserotypic variation in the Streptococcus pyogenes Rgg regulon. FEMS Microbiol Lett 284:43–51
    [Google Scholar]
  15. Echenique J. R., Trombe M. C. 2001; Competence repression under oxygen limitation through the two-component MicAB signal-transducing system in Streptococcus pneumoniae and involvement of the PAS domain of MicB. J Bacteriol 183:4599–4608
    [Google Scholar]
  16. Echenique J. R., Chapuy-Regaud S., Trombe M. C. 2000; Competence regulation by oxygen in Streptococcus pneumoniae: involvement of ciaRH and comCDE . Mol Microbiol 36:688–696
    [Google Scholar]
  17. Giuliodori A. M., Gualerzi C. O., Soto S., Vila J., Tavio M. M. 2007; Review on bacterial stress topics. Ann N Y Acad Sci 111395–104
    [Google Scholar]
  18. Green G. H., Diggle P. J. 2007; On the operational characteristics of the Benjamini and Hochberg false discovery rate procedure. Stat Appl Genet Mol Biol 6:Article27
    [Google Scholar]
  19. Horton R. M., Cai Z. L., Ho S. N., Pease L. R. 1990; Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8:528–535
    [Google Scholar]
  20. Hoskins J., Alborn W. E. Jr, Arnold J., Blaszczak L. C., Burgett S., DeHoff B. S., Estrem S. T., Fritz L., Fu D. J. other authors 2001; Genome of the bacterium Streptococcus pneumoniae strain R6. J Bacteriol 183:5709–5717
    [Google Scholar]
  21. Houot L., Watnick P. I. 2008; A novel role for enzyme I of the Vibrio cholerae phosphoenolpyruvate phosphotransferase system in regulation of growth in a biofilm. J Bacteriol 190:311–320
    [Google Scholar]
  22. Kadioglu A., Weiser J. N., Paton J. C., Andrew P. W. 2008; The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat Rev Microbiol 6:288–301
    [Google Scholar]
  23. Kreikemeyer B., McIver K. S., Podbielski A. 2003; Virulence factor regulation and regulatory networks in Streptococcus pyogenes and their impact on pathogen–host interactions. Trends Microbiol 11:224–232
    [Google Scholar]
  24. Lampe D. J., Churchill M. E., Robertson H. M. 1996; A purified mariner transposase is sufficient to mediate transposition in vitro . EMBO J 15:5470–5479
    [Google Scholar]
  25. Lanie J. A., Ng W. L., Kazmierczak K. M., Andrzejewski T. M., Davidsen T. M., Wayne K. J., Tettelin H., Glass J. I., Winkler M. E. 2007; Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J Bacteriol 189:38–51
    [Google Scholar]
  26. Livak K. J., Schmittgen T. D. 2001; Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408
    [Google Scholar]
  27. Martin B., Prudhomme M., Alloing G., Granadel C., Claverys J. P. 2000; Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae . Mol Microbiol 38:867–878
    [Google Scholar]
  28. Martin-Galiano A. J., Overweg K., Ferrandiz M. J., Reuter M., Wells J. M., de la Campa A. G. 2005; Transcriptional analysis of the acid tolerance response in Streptococcus pneumoniae . Microbiology 151:3935–3946
    [Google Scholar]
  29. McCluskey J., Hinds J., Husain S., Witney A., Mitchell T. J. 2004; A two-component system that controls the expression of pneumococcal surface antigen A (PsaA) and regulates virulence and resistance to oxidative stress in Streptococcus pneumoniae . Mol Microbiol 51:1661–1675
    [Google Scholar]
  30. McDougald D., Gong L., Srinivasan S., Hild E., Thompson L., Takayama K., Rice S. A., Kjelleberg S. 2002; Defences against oxidative stress during starvation in bacteria. Antonie Van Leeuwenhoek 81:3–13
    [Google Scholar]
  31. Mongkolsuk S., Helmann J. D. 2002; Regulation of inducible peroxide stress responses. Mol Microbiol 45:9–15
    [Google Scholar]
  32. Morton D. B. 1985; Pain and laboratory animals. Nature 317:106
    [Google Scholar]
  33. Moscoso M., Garcia E., Lopez R. 2006; Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion. J Bacteriol 188:7785–7795
    [Google Scholar]
  34. Mostertz J., Scharf C., Hecker M., Homuth G. 2004; Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. Microbiology 150:497–512
    [Google Scholar]
  35. Muñoz-Elías E. J., Marcano J., Camilli A. 2008; Isolation of Streptococcus pneumoniae biofilm mutants and their characterization during nasopharyngeal colonization. Infect Immun 76:5049–5061
    [Google Scholar]
  36. Neves A. R., Pool W. A., Kok J., Kuipers O. P., Santos H. 2005; Overview on sugar metabolism and its control in Lactococcus lactis – the input from in vivo NMR. FEMS Microbiol Rev 29:531–554
    [Google Scholar]
  37. Oggioni M. R., Trappetti C., Kadioglu A., Cassone M., Iannelli F., Ricci S., Andrew P. W., Pozzi G. 2006; Switch from planktonic to sessile life: a major event in pneumococcal pathogenesis. Mol Microbiol 61:1196–1210
    [Google Scholar]
  38. Ogura M., Yamaguchi H., Kobayashi K., Ogasawara N., Fujita Y., Tanaka T. 2002; Whole-genome analysis of genes regulated by the Bacillus subtilis competence transcription factor ComK. J Bacteriol 184:2344–2351
    [Google Scholar]
  39. Orihuela C. J., Radin J. N., Sublett J. E., Gao G., Kaushal D., Tuomanen E. I. 2004; Microarray analysis of pneumococcal gene expression during invasive disease. Infect Immun 72:5582–5596
    [Google Scholar]
  40. Paterson G. K., Blue C. E., Mitchell T. J. 2006; An operon in Streptococcus pneumoniae containing a putative alkylhydroperoxidase D homologue contributes to virulence and the response to oxidative stress. Microb Pathog 40:152–160
    [Google Scholar]
  41. Pericone C. D., Park S., Imlay J. A., Weiser J. N. 2003; Factors contributing to hydrogen peroxide resistance in Streptococcus pneumoniae include pyruvate oxidase (SpxB) and avoidance of the toxic effects of the Fenton reaction. J Bacteriol 185:6815–6825
    [Google Scholar]
  42. Pesakhov S., Benisty R., Sikron N., Cohen Z., Gomelsky P., Khozin-Goldberg I., Dagan R., Porat N. 2007; Effect of hydrogen peroxide production and the Fenton reaction on membrane composition of Streptococcus pneumoniae . Biochim Biophys Acta 1768:590–597
    [Google Scholar]
  43. Pestova E. V., Morrison D. A. 1998; Isolation and characterization of three Streptococcus pneumoniae transformation-specific loci by use of a lacZ reporter insertion vector. J Bacteriol 180:2701–2710
    [Google Scholar]
  44. Pulliainen A. T., Hytonen J., Haataja S., Finne J. 2008; Deficiency of the Rgg regulator promotes H2O2 resistance, AhpCF-mediated H2O2 decomposition, and virulence in Streptococcus pyogenes . J Bacteriol 190:3225–3235
    [Google Scholar]
  45. Rimini R., Jansson B., Feger G., Roberts T. C., de Francesco M., Gozzi A., Faggioni F., Domenici E., Wallace D. M. other authors 2000; Global analysis of transcription kinetics during competence development in Streptococcus pneumoniae using high density DNA arrays. Mol Microbiol 36:1279–1292
    [Google Scholar]
  46. Rocha E. R., Selby T., Coleman J. P., Smith C. J. 1996; Oxidative stress response in an anaerobe, Bacteroides fragilis: a role for catalase in protection against hydrogen peroxide. J Bacteriol 178:6895–6903
    [Google Scholar]
  47. Samen U. M., Eikmanns B. J., Reinscheid D. J. 2006; The transcriptional regulator RovS controls the attachment of Streptococcus agalactiae to human epithelial cells and the expression of virulence genes. Infect Immun 74:5625–5635
    [Google Scholar]
  48. Sicard A. M. 1964; A new synthetic medium for Diplococcus pneumoniae, and its use for the study of reciprocal transformations at the amiA locus. Genetics 50:31–44
    [Google Scholar]
  49. Spellerberg B., Cundell D. R., Sandros J., Pearce B. J., Idanpaan-Heikkila I., Rosenow C., Masure H. R. 1996; Pyruvate oxidase, as a determinant of virulence in Streptococcus pneumoniae . Mol Microbiol 19:803–813
    [Google Scholar]
  50. Stewart G. R., Wernisch L., Stabler R., Mangan J. A., Hinds J., Laing K. G., Young D. B., Butcher P. D. 2002; Dissection of the heat-shock response in Mycobacterium tuberculosis using mutants and microarrays. Microbiology 148:3129–3138
    [Google Scholar]
  51. Tettelin H., Masignani V., Cieslewicz M. J., Eisen J. A., Peterson S., Wessels M. R., Paulsen I. T., Nelson K. E., Margarit I. other authors 2002; Complete genome sequence and comparative genomic analysis of an emerging human pathogen, serotype V Streptococcus agalactiae . Proc Natl Acad Sci U S A 99:12391–12396
    [Google Scholar]
  52. Torrents E., Eliasson R., Wolpher H., Graslund A., Reichard P. 2001; The anaerobic ribonucleotide reductase from Lactococcus lactis. Interactions between the two proteins NrdD and NrdG. J Biol Chem 276:33488–33494
    [Google Scholar]
  53. Touati D. 2000; Iron and oxidative stress in bacteria. Arch Biochem Biophys 373:1–6
    [Google Scholar]
  54. Tseng H. J., McEwan A. G., Paton J. C., Jennings M. P. 2002; Virulence of Streptococcus pneumoniae: PsaA mutants are hypersensitive to oxidative stress. Infect Immun 70:1635–1639
    [Google Scholar]
  55. Ulijasz A. T., Andes D. R., Glasner J. D., Weisblum B. 2004; Regulation of iron transport in Streptococcus pneumoniae by RitR, an orphan response regulator. J Bacteriol 186:8123–8136
    [Google Scholar]
  56. Vergauwen B., Pauwels F., Van Beeumen J. J. 2003; Glutathione and catalase provide overlapping defenses for protection against respiration-generated hydrogen peroxide in Haemophilus influenzae . J Bacteriol 185:5555–5562
    [Google Scholar]
  57. Vickerman M. M., Wang M., Baker L. J. 2003; An amino acid change near the carboxyl terminus of the Streptococcus gordonii regulatory protein Rgg affects its abilities to bind DNA and influence expression of the glucosyltransferase gene gtfG . Microbiology 149:399–406
    [Google Scholar]
  58. Weiser J. N., Bae D., Epino H., Gordon S. B., Kapoor M., Zenewicz L. A., Shchepetov M. 2001; Changes in availability of oxygen accentuate differences in capsular polysaccharide expression by phenotypic variants and clinical isolates of Streptococcus pneumoniae . Infect Immun 69:5430–5439
    [Google Scholar]
  59. Yesilkaya H., Kadioglu A., Gingles N., Alexander J. E., Mitchell T. J., Andrew P. W. 2000; Role of manganese-containing superoxide dismutase in oxidative stress and virulence of Streptococcus pneumoniae . Infect Immun 68:2819–2826
    [Google Scholar]
  60. Yesilkaya H., Forbes K. J., Shafi J., Smith R., Dale J. W., Rajakumar K., Barer M. R., Andrew P. W. 2006; The genetic portrait of an outbreak strain. Tuberculosis (Edinb ) 86:357–362
    [Google Scholar]
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