1887

Microbiology

Volume 158, Issue 9

Peroxide resistance in serotype O157 : H7 biofilms is regulated by both RpoS-dependent and -independent mechanisms Free

Abstract

In many serotype O157 : H7 strains, defences against peroxide damage include the peroxiredoxin AhpCF and three catalases: KatG (catalase/peroxidase), KatE (catalase) and the plasmid-encoded KatP (catalase/peroxidase). AhpC and KatG basal expression is maintained by RpoS, and AhpC, KatG and KatP are all induced by OxyR/σ in exponential phase. KatE is regulated by RpoS during stationary growth and is independent of OxyR. In a previous study we used mutant strains of ATCC 43895 (EDL933) with deletions of , , and in all possible combinations to characterize peroxide resistance during both exponential and 18–24 h growth in Luria–Bertani broth at 37 °C. In this study, we used triple deletion strains that isolated each catalase/peroxidase gene to investigate their role in the peroxide resistance of biofilm-forming variant 43895OR in 48 and 72 h biofilms. We also used quantitative real-time reverse transcriptase PCR and translational fusions to study gene expression. Peroxide resistance was greater (<0.05) in biofilm cells than in planktonic cells, and full resistance required but not . In 72 h biofilms, and were the major protective genes. , and peroxide protection had both -dependent and -independent components, but protection was independent of . HO challenge induced (<0.05) , expression in biofilm cells, suggesting that peroxide induction of the OxyR-dependent resistance genes may contribute to the RpoS-independent protection in Shiga toxin-producing biofilms.

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  • Accepted:
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2012-09-01
2021-01-19
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References

  1. Altuvia S., Almirón M., Huisman G., Kolter R., Storz G.. ( 1994;). The dps promoter is activated by OxyR during growth and by IHF and σS in stationary phase. Mol Microbiol13:265–272 [CrossRef][PubMed]
     [Google Scholar]
  2. Barnhart M. M., Chapman M. R.. ( 2006;). Curli biogenesis and function. Annu Rev Microbiol60:131–147 [CrossRef][PubMed]
     [Google Scholar]
  3. Brunder W., Schmidt H., Karch H.. ( 1996;). KatP, a novel catalase-peroxidase encoded by the large plasmid of enterohaemorrhagic Escherichia coli O157 : H7. Microbiology142:3305–3315 [CrossRef][PubMed]
     [Google Scholar]
  4. Cochran W. L., McFeters G. A., Stewart P. S.. ( 2000;). Reduced susceptibility of thin Pseudomonas aeruginosa biofilms to hydrogen peroxide and monochloramine. J Appl Microbiol88:22–30 [CrossRef][PubMed]
     [Google Scholar]
  5. Coldewey S. M., Hartmann M., Schmidt D. S., Engelking U., Ukena S. N., Gunzer F.. ( 2007;). Impact of the rpoS genotype for acid resistance patterns of pathogenic and probiotic Escherichia coli. BMC Microbiol7:21 [CrossRef][PubMed]
     [Google Scholar]
  6. Ferenci T.. ( 2003;). What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli?. Trends Microbiol11:457–461 [CrossRef][PubMed]
     [Google Scholar]
  7. González-Flecha B., Demple B.. ( 1995;). Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J Biol Chem270:13681–13687 [CrossRef][PubMed]
     [Google Scholar]
  8. González-Flecha B., Demple B.. ( 1997a;). Homeostatic regulation of intracellular hydrogen peroxide concentration in aerobically growing Escherichia coli. J Bacteriol179:382–388[PubMed]
     [Google Scholar]
  9. González-Flecha B., Demple B.. ( 1997b;). Transcriptional regulation of the Escherichia coli oxyR gene as a function of cell growth. J Bacteriol179:6181–6186[PubMed]
     [Google Scholar]
  10. Hammar M., Bian Z., Normark S.. ( 1996;). Nucleator-dependent intercellular assembly of adhesive curli organelles in Escherichia coli. Proc Natl Acad Sci U S A93:6562–6566 [CrossRef][PubMed]
     [Google Scholar]
  11. Imlay J. A.. ( 2008;). Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem77:755–776 [CrossRef][PubMed]
     [Google Scholar]
  12. Jung I. L., Kim I. G.. ( 2003;). Transcription of ahpC, katG, and katE genes in Escherichia coli is regulated by polyamines: polyamine-deficient mutant sensitive to H2O2-induced oxidative damage. Biochem Biophys Res Commun301:915–922 [CrossRef][PubMed]
     [Google Scholar]
  13. Livak K. J., Schmittgen T. D.. ( 2001;). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔ C T method. Methods25:402–408 [CrossRef][PubMed]
     [Google Scholar]
  14. Miller J. H.. ( 1972;). Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  15. Miller R. G.. ( 1981;). Simultaneous Statistical Inference, 2nd edn.67–70 New York: Spinger-Verlag;
     [Google Scholar]
  16. Morgan R. W., Christman M. F., Jacobson F. S., Storz G., Ames B. N.. ( 1986;). Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proc Natl Acad Sci U S A83:8059–8063 [CrossRef][PubMed]
     [Google Scholar]
  17. Mukhopadhyay S., Schellhorn H. E.. ( 1994;). Induction of Escherichia coli hydroperoxidase I by acetate and other weak acids. J Bacteriol176:2300–2307[PubMed]
     [Google Scholar]
  18. Mulvey M. R., Switala J., Borys A., Loewen P. C.. ( 1990;). Regulation of transcription of katE and katF in Escherichia coli. J Bacteriol172:6713–6720[PubMed]
     [Google Scholar]
  19. Notley-McRobb L., King T., Ferenci T.. ( 2002;). rpoS mutations and loss of general stress resistance in Escherichia coli populations as a consequence of conflict between competing stress responses. J Bacteriol184:806–811 [CrossRef][PubMed]
     [Google Scholar]
  20. Park S., You X., Imlay J. A.. ( 2005;). Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx− mutants of Escherichia coli. Proc Natl Acad Sci U S A102:9317–9322 [CrossRef][PubMed]
     [Google Scholar]
  21. Poirier K., Faucher S. P., Béland M., Brousseau R., Gannon V., Martin C., Harel J., Daigle F.. ( 2008;). Escherichia coli O157 : H7 survives within human macrophages: global gene expression profile and involvement of the Shiga toxins. Infect Immun76:4814–4822 [CrossRef][PubMed]
     [Google Scholar]
  22. Robey M., Benito A., Hutson R. H., Pascual C., Park S. F., Mackey B. M.. ( 2001;). Variation in resistance to high hydrostatic pressure and rpoS heterogeneity in natural isolates of Escherichia coli O157 : H7. Appl Environ Microbiol67:4901–4907 [CrossRef][PubMed]
     [Google Scholar]
  23. Ryu J.-H., Kim H., Frank J. F., Beuchat L. R.. ( 2004;). Attachment and biofilm formation on stainless steel by Escherichia coli O157 : H7 as affected by curli production. Lett Appl Microbiol39:359–362 [CrossRef][PubMed]
     [Google Scholar]
  24. Schellhorn H. E., Hassan H. M.. ( 1988;). Transcriptional regulation of katE in Escherichia coli K-12. J Bacteriol170:4286–4292[PubMed]
     [Google Scholar]
  25. Schellhorn H. E., Stones V. L.. ( 1992;). Regulation of katF and katE in Escherichia coli K-12 by weak acids. J Bacteriol174:4769–4776[PubMed]
     [Google Scholar]
  26. Seaver L. C., Imlay J. A.. ( 2001;). Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol183:7173–7181 [CrossRef][PubMed]
     [Google Scholar]
  27. Stewart P. S., Franklin M. J.. ( 2008;). Physiological heterogeneity in biofilms. Nat Rev Microbiol6:199–210 [CrossRef][PubMed]
     [Google Scholar]
  28. Stewart P. S., Roe F., Rayner J., Elkins J. G., Lewandowski Z., Ochsner U. A., Hassett D. J.. ( 2000;). Effect of catalase on hydrogen peroxide penetration into Pseudomonas aeruginosa biofilms. Appl Environ Microbiol66:836–838 [CrossRef][PubMed]
     [Google Scholar]
  29. Storz G., Tartaglia L. A.. ( 1992;). OxyR: a regulator of antioxidant genes. J Nutr122:Suppl. 3627–630[PubMed]
     [Google Scholar]
  30. Uhlich G. A.. ( 2009;). KatP contributes to OxyR-regulated hydrogen peroxide resistance in Escherichia coli serotype O157 : H7. Microbiology155:3589–3598 [CrossRef][PubMed]
     [Google Scholar]
  31. Uhlich G. A., Keen J. E., Elder R. O.. ( 2001;). Mutations in the csgD promoter associated with variations in curli expression in certain strains of Escherichia coli O157 : H7. Appl Environ Microbiol67:2367–2370 [CrossRef][PubMed]
     [Google Scholar]
  32. Uhlich G. A., Keen J. E., Elder R. O.. ( 2002;). Variations in the csgD promoter of Escherichia coli O157 : H7 associated with increased virulence in mice and increased invasion of HEp-2 cells. Infect Immun70:395–399 [CrossRef][PubMed]
     [Google Scholar]
  33. Uhlich G. A., Cooke P. H., Solomon E. B.. ( 2006;). Analyses of the red-dry-rough phenotype of an Escherichia coli O157 : H7 strain and its role in biofilm formation and resistance to antibacterial agents. Appl Environ Microbiol72:2564–2572 [CrossRef][PubMed]
     [Google Scholar]
  34. Uhlich G. A., Rogers D. P., Mosier D. A.. ( 2010;). Escherichia coli serotype O157 : H7 retention on solid surfaces and peroxide resistance is enhanced by dual-strain biofilm formation. Foodborne Pathog Dis7:935–943 [CrossRef][PubMed]
     [Google Scholar]
  35. Visick J. E., Clarke S.. ( 1997;). RpoS- and OxyR-independent induction of HPI catalase at stationary phase in Escherichia coli and identification of rpoS mutations in common laboratory strains. J Bacteriol179:4158–4163[PubMed]
     [Google Scholar]
  36. Waterman S. R., Small P. L. C.. ( 1996;). Characterization of the acid resistance phenotype and rpoS alleles of Shiga-like toxin-producing Escherichia coli. Infect Immun64:2808–2811[PubMed]
     [Google Scholar]
  37. Zambrano M. M., Siegele D. A., Almirón M., Tormo A., Kolter R.. ( 1993;). Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science259:1757–1760 [CrossRef][PubMed]
     [Google Scholar]
  38. Zar J. H.. ( 1999;). Biostatistical Analysis, 4th edn.210–214 Upper Saddle River, NJ: Prentice Hall;
     [Google Scholar]
  39. 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 Bacteriol183:4562–4570 [CrossRef][PubMed]
     [Google Scholar]
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Peroxide resistance in Escherichia coli serotype O157 : H7 biofilms is regulated by both RpoS-dependent and -independent mechanisms
Microbiology 158, 2225 (2012); https://doi.org/10.1099/mic.0.059535-0
/content/journal/micro/10.1099/mic.0.059535-0
/content/journal/micro/10.1099/mic.0.059535-0
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