1887

Abstract

Hydrogen peroxide (HO), an important substance produced by many members of the genus , plays important roles in virulence and antagonism within a microbial community such as oral biofilms. The gene, which encodes pyruvate oxidase, is involved in HO production in many streptococcal species. However, knowledge about its regulation and relation with other genes putatively involved in the same pathway is limited. In this study, three genes – and – were identified as contributing to HO production in by screening mutants for opaque colony appearance. Mutations in all three genes resulted in significant decreases in HO production, with 16–31 % of that of the wild-type. HO production was restored in the complemented strains. Antagonism against by these three mutants was reduced, both on plates and in liquid cultures, indicating the critical roles of these three genes for conferring the competitive advantage of Analysis by qPCR indicated that the expression of was decreased in the and mutants and significantly increased in the mutant.

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2011-01-01
2024-04-26
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References

  1. Auzat I., Chapuy-Regaud S., Le Bras G., Dos S. D., Ogunniyi A. D., Le T. 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]
  2. Becker M. R., Paster B. J., Leys E. J., Moeschberger M. L., Kenyon S. G., Galvin J. L., Boches S. K., Dewhirst F. E., Griffen A. L. 2002; Molecular analysis of bacterial species associated with childhood caries. J Clin Microbiol 40:1001–1009
    [Google Scholar]
  3. Belanger A. E., Clague M. J., Glass J. I., LeBlanc D. J. 2004; Pyruvate oxidase is a determinant of Avery's rough morphology. J Bacteriol 186:8164–8171
    [Google Scholar]
  4. Carlsson J., Kujala U. 1984; Pyruvate oxidase activity dependent on thiamine pyrophosphate, flavin adenine dinucleotide and orthophosphate in Streptococcus sanguis . FEMS Microbiol Lett 25:53–56
    [Google Scholar]
  5. Caufield P. W., Dasanayake A. P., Li Y., Pan Y., Hsu J., Hardin J. M. 2000; Natural history of Streptococcus sanguinis in the oral cavity of infants: evidence for a discrete window of infectivity. Infect Immun 68:4018–4023
    [Google Scholar]
  6. Douglas C. W., Heath J., Hampton K. K., Preston F. E. 1993; Identity of viridans streptococci isolated from cases of infective endocarditis. J Med Microbiol 39:179–182
    [Google Scholar]
  7. García-Mendoza A., Liebana J., Castillo A. M., de la Higuera A., Piedrola G. 1993; Evaluation of the capacity of oral streptococci to produce hydrogen peroxide. J Med Microbiol 39:434–439
    [Google Scholar]
  8. Ge X., Kitten T., Chen Z., Lee S. P., Munro C. L., Xu P. 2008a; Identification of Streptococcus sanguinis genes required for biofilm formation and examination of their role in endocarditis virulence. Infect Immun 76:2551–2559
    [Google Scholar]
  9. Ge Y., Caufield P. W., Fisch G. S., Li Y. 2008b; Streptococcus mutans and Streptococcus sanguinis colonization correlated with caries experience in children. Caries Res 42:444–448
    [Google Scholar]
  10. Ginsburg I., Sadovnic M. 1998; Gamma globulin, Evan's blue, aprotinin A PLA2 inhibitor, tetracycline and antioxidants protect epithelial cells against damage induced by synergism among streptococcal hemolysins, oxidants and proteinases: relation to the prevention of post-streptococcal sequelae and septic shock. FEMS Immunol Med Microbiol 22:247–256
    [Google Scholar]
  11. Ginsburg I., Varani J. 1993; Interaction of viable group A streptococci and hydrogen peroxide in killing of vascular endothelial cells. Free Radic Biol Med 14:495–500
    [Google Scholar]
  12. Gorrell A., Lawrence S. H., Ferry J. G. 2005; Structural and kinetic analyses of arginine residues in the active site of the acetate kinase from Methanosarcina thermophila . J Biol Chem 280:10731–10742
    [Google Scholar]
  13. Jakubovics N. S., Smith A. W., Jenkinson H. F. 2002; Oxidative stress tolerance is manganese (Mn2+) regulated in Streptococcus gordonii . Microbiology 148:3255–3263
    [Google Scholar]
  14. Kemp B. E. 2004; Bateman domains and adenosine derivatives form a binding contract. J Clin Invest 113:182–184
    [Google Scholar]
  15. Kilian M., Holmgren K. 1981; Ecology and nature of immunoglobulin A1 protease-producing streptococci in the human oral cavity and pharynx. Infect Immun 31:868–873
    [Google Scholar]
  16. Kreth J., Merritt J., Shi W., Qi F. 2005; Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J Bacteriol 187:7193–7203
    [Google Scholar]
  17. Kreth J., Zhang Y., Herzberg M. C. 2008; Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans . J Bacteriol 190:4632–4640
    [Google Scholar]
  18. Kreth J., Vu H., Zhang Y., Herzberg M. C. 2009; Characterization of hydrogen peroxide-induced DNA release by Streptococcus sanguinis and Streptococcus gordonii . J Bacteriol 191:6281–6291
    [Google Scholar]
  19. Kuramitsu H. K., He X., Lux R., Anderson M. H., Shi W. 2007; Interspecies interactions within oral microbial communities. Microbiol Mol Biol Rev 71:653–670
    [Google Scholar]
  20. Muller Y. A., Schumacher G., Rudolph R., Schulz G. E. 1994; The refined structures of a stabilized mutant and of wild-type pyruvate oxidase from Lactobacillus plantarum . J Mol Biol 237:315–335
    [Google Scholar]
  21. Mylonakis E., Calderwood S. B. 2001; Infective endocarditis in adults. N Engl J Med 345:1318–1330
    [Google Scholar]
  22. Overweg K., Pericone C. D., Verhoef G. G. C., Weiser J. N., Meiring H. D., De Jong A. P. J. M., De Groot R., Hermans P. W. M. 2000; Differential protein expression in phenotypic variants of Streptococcus pneumoniae . Infect Immun 68:4604–4610
    [Google Scholar]
  23. Paik S., Senty L., Das S., Noe J. C., Munro C. L., Kitten T. 2005; Identification of virulence determinants for endocarditis in Streptococcus sanguinis by signature-tagged mutagenesis. Infect Immun 73:6064–6074
    [Google Scholar]
  24. Pericone C. D., Overweg K., Hermans P. W. M., Weiser J. N. 2000; Inhibitory and bactericidal effects of hydrogen peroxide production by Streptococcus pneumoniae on other inhabitants of the upper respiratory tract. Infect Immun 68:3990–3997
    [Google Scholar]
  25. Pericone C. D., Bae D., Shchepetov M., McCool T., Weiser J. N. 2002; Short-sequence tandem and nontandem DNA repeats and endogenous hydrogen peroxide production contribute to genetic instability of Streptococcus pneumoniae . J Bacteriol 184:4392–4399
    [Google Scholar]
  26. Ramos-Montañez S., Tsui H. C., Wayne K. J., Morris J. L., Peters L. E., Zhang F., Kazmierczak K. M., Sham L. T., Winkler M. E. 2008; Polymorphism and regulation of the spxB (pyruvate oxidase) virulence factor gene by a CBS-HotDog domain protein (SpxR) in serotype 2 Streptococcus pneumoniae . Mol Microbiol 67:729–746
    [Google Scholar]
  27. Rigali S., Derouaux A., Giannotta F., Dusart J. 2002; Subdivision of the helix–turn–helix GntR family of bacterial regulators in the FadR, HutC, MocR, and YtrA subfamilies. J Biol Chem 277:12507–12515
    [Google Scholar]
  28. Rosan B., Lamont R. J. 2000; Dental plaque formation. Microbes Infect 2:1599–1607
    [Google Scholar]
  29. Scott J. W., Hawley S. A., Green K. A., Anis M., Stewart G., Scullion G. A., Norman D. G., Hardie D. G. 2004; CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J Clin Invest 113:274–284
    [Google Scholar]
  30. Tittmann K., Proske D., Spinka M., Ghisla S., Rudolph R., Hubner G., Kern G. 1998; Activation of thiamin diphosphate and FAD in the phosphate-dependent pyruvate oxidase from Lactobacillus plantarum . J Biol Chem 273:12929–12934
    [Google Scholar]
  31. Tittmann K., Wille G., Golbik R., Weidner A., Ghisla S., Hubner G. 2005; Radical phosphate transfer mechanism for the thiamin diphosphate- and FAD-dependent pyruvate oxidase from Lactobacillus plantarum . Kinetic coupling of intercofactor electron transfer with phosphate transfer to acetyl-thiamin diphosphate via a transient FAD semiquinone/hydroxyethyl-ThDP radical pair. Biochemistry 44:13291–13303
    [Google Scholar]
  32. Tleyjeh I. M., Steckelberg J. M., Murad H. S., Anavekar N. S., Ghomrawi H. M., Mirzoyev Z., Moustafa S. E., Hoskin T. L., Mandrekar J. N. other authors 2005; Temporal trends in infective endocarditis: a population-based study in Olmsted County, Minnesota. JAMA 293:3022–3028
    [Google Scholar]
  33. Turner L. S., Das S., Kanamoto T., Munro C. L., Kitten T. 2009; Development of genetic tools for in vivo virulence analysis of Streptococcus sanguinis . Microbiology 155:2573–2582
    [Google Scholar]
  34. Uehara Y., Agematsu K., Kikuchi K., Matsuzaki S., Imai S., Takamoto M., Sugane K., Sugiura T., Konishi Y. other authors 2006; Secretory IgA, salivary peroxidase, and catalase-mediated microbicidal activity during hydrogen peroxide catabolism in viridans streptococci: pathogen coaggregation. J Infect Dis 194:98–107
    [Google Scholar]
  35. Wang H., Tseng C. P., Gunsalus R. P. 1999; The napF and narG nitrate reductase operons in Escherichia coli are differentially expressed in response to submicromolar concentrations of nitrate but not nitrite. J Bacteriol 181:5303–5308
    [Google Scholar]
  36. Weiser J. N., Austrian R., Sreenivasan P. K., Masure H. R. 1994; Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization. Infect Immun 62:2582–2589
    [Google Scholar]
  37. Xu P., Alves J. M., Kitten T., Brown A., Chen Z., Ozaki L. S., Manque P., Ge X., Serrano M. G. other authors 2007; Genome of the opportunistic pathogen Streptococcus sanguinis . J Bacteriol 189:3166–3175
    [Google Scholar]
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