1887

Abstract

Biofilm formation in is a tightly controlled process requiring the expression of adhesive curli fibres and certain polysaccharides such as cellulose. The transcriptional regulator CsgD is central to biofilm formation, controlling the expression of the curli structural and export proteins and the diguanylate cyclase , which indirectly activates cellulose production. CsgD itself is highly regulated by two sigma factors (RpoS and RpoD), multiple DNA-binding proteins, small regulatory RNAs and several GGDEF/EAL proteins acting through c-di-GMP. One such transcription factor MlrA binds the promoter to enhance the RpoS-dependent transcription of . Bacteriophage, often carrying the gene, utilize an insertion site in the proximal coding region of serotype O157 : H7 strains, and the loss of function would be expected to be the major factor contributing to poor curli and biofilm expression in that serotype. Using a bank of 55 strains of serotype O157 : H7, we investigated the consequences of bacteriophage insertion. Although curli/biofilm expression was restored in many of the prophage-bearing strains by a wild-type copy of on a multi-copy plasmid, more than half of the strains showed only partial or no complementation. Moreover, the two strains carrying an intact were found to be deficient in biofilm formation. However, RpoS mutations that attenuated or inactivated RpoS-dependent functions such as biofilm formation were found in >70 % of the strains, including the two strains with an intact . We conclude that bacteriophage interruption of and RpoS mutations provide major obstacles limiting curli expression and biofilm formation in most serotype O157 : H7 strains.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.066118-0
2013-08-01
2019-12-11
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/8/1586.html?itemId=/content/journal/micro/10.1099/mic.0.066118-0&mimeType=html&fmt=ahah

References

  1. Beutin L. , Montenegro M. A. , Orskov I. , Orskov F. , Prada J. , Zimmermann S. , Stephan R. . ( 1989; ). Close association of verotoxin (Shiga-like toxin) production with enterohemolysin production in strains of Escherichia coli. . J Clin Microbiol 27:, 2559–2564.[PubMed]
    [Google Scholar]
  2. Bokranz W. , Wang X. , Tschäpe H. , Römling U. . ( 2005; ). Expression of cellulose and curli fimbriae by Escherichia coli isolated from the gastrointestinal tract. . J Med Microbiol 54:, 1171–1182. [CrossRef] [PubMed]
    [Google Scholar]
  3. Bougdour A. , Lelong C. , Geiselmann J. . ( 2004; ). Crl, a low temperature-induced protein in Escherichia coli that binds directly to the stationary phase σ subunit of RNA polymerase. . J Biol Chem 279:, 19540–19550. [CrossRef] [PubMed]
    [Google Scholar]
  4. Brown P. K. , Dozois C. M. , Nickerson C. A. , Zuppardo A. , Terlonge J. , Curtiss R. III . ( 2001; ). MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar Typhimurium. . Mol Microbiol 41:, 349–363. [CrossRef] [PubMed]
    [Google Scholar]
  5. Carter M. Q. , Brandl M. T. , Louie J. W. , Kyle J. L. , Carychao D. K. , Cooley M. B. , Parker C. T. , Bates A. H. , Mandrell R. E. . ( 2011; ). Distinct acid resistance and survival fitness displayed by curli variants of enterohemorrhagic Escherichia coli O157:H7. . Appl Environ Microbiol 77:, 3685–3695. [CrossRef] [PubMed]
    [Google Scholar]
  6. 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 Microbiol 7:, 21. [CrossRef] [PubMed]
    [Google Scholar]
  7. Dorel C. , Lejeune P. , Rodrigue A. . ( 2006; ). The Cpx system of Escherichia coli, a strategic signaling pathway for confronting adverse conditions and for settling biofilm communities?. Res Microbiol 157:, 306–314. [CrossRef] [PubMed]
    [Google Scholar]
  8. Ferenci T. . ( 2003; ). What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli? . Trends Microbiol 11:, 457–461. [CrossRef] [PubMed]
    [Google Scholar]
  9. Ferrières L. , Clarke D. J. . ( 2003; ). The RcsC sensor kinase is required for normal biofilm formation in Escherichia coli K-12 and controls the expression of a regulon in response to growth on a solid surface. . Mol Microbiol 50:, 1665–1682. [CrossRef] [PubMed]
    [Google Scholar]
  10. Galhardo R. S. , Hastings P. J. , Rosenberg S. M. . ( 2007; ). Mutation as a stress response and the regulation of evolvability. . Crit Rev Biochem Mol Biol 42:, 399–435. [CrossRef] [PubMed]
    [Google Scholar]
  11. Gerstel U. , Römling U. . ( 2003; ). The csgD promoter, a control unit for biofilm formation in Salmonella typhimurium. . Res Microbiol 154:, 659–667. [CrossRef] [PubMed]
    [Google Scholar]
  12. Gerstel U. , Park C. , Römling U. . ( 2003; ). Complex regulation of csgD promoter activity by global regulatory proteins. . Mol Microbiol 49:, 639–654. [CrossRef] [PubMed]
    [Google Scholar]
  13. Gualdi L. , Tagliabue L. , Landini P. . ( 2007; ). Biofilm formation-gene expression relay system in Escherichia coli: modulation of σs-dependent gene expression by the CsgD regulatory protein via σs-protein stabilization. . J Bacteriol 189:, 8034–8043. [CrossRef] [PubMed]
    [Google Scholar]
  14. Hartzell A. , Chen C. , Lewis C. , Liu K. , Reynolds S. , Dudley E. G. . ( 2011; ). Escherichia coli O157:H7 of genotype lineage-specific polymorphism assay 211111 and clade 8 are common clinical isolates within Pennsylvania. . Foodborne Pathog Dis 8:, 763–768. [CrossRef] [PubMed]
    [Google Scholar]
  15. Holmqvist E. , Reimegård J. , Sterk M. , Grantcharova N. , Römling U. , Wagner E. G. H. . ( 2010; ). Two antisense RNAs target the transcriptional regulator CsgD to inhibit curli synthesis. . EMBO J 29:, 1840–1850. [CrossRef] [PubMed]
    [Google Scholar]
  16. Jackson D. W. , Simecka J. W. , Romeo T. . ( 2002; ). Catabolite repression of Escherichia coli biofilm formation. . J Bacteriol 184:, 3406–3410. [CrossRef] [PubMed]
    [Google Scholar]
  17. Jørgensen M. G. , Nielsen J. S. , Boysen A. , Franch T. , Møller-Jensen J. , Valentin-Hansen P. . ( 2012; ). Small regulatory RNAs control the multi-cellular adhesive lifestyle of Escherichia coli. . Mol Microbiol 84:, 36–50. [CrossRef] [PubMed]
    [Google Scholar]
  18. Liu X. , Matsumura P. . ( 1994; ). The FlhD/FlhC complex, a transcriptional activator of the Escherichia coli flagellar class II operons. . J Bacteriol 176:, 7345–7351.[PubMed]
    [Google Scholar]
  19. Mika F. , Busse S. , Possling A. , Berkholz J. , Tschowri N. , Sommerfeldt N. , Pruteanu M. , Hengge R. . ( 2012; ). Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli . . Mol Microbiol 84:, 51–65. [CrossRef] [PubMed]
    [Google Scholar]
  20. Neumann B. , Pospiech A. , Schairer H. U. . ( 1992; ). Rapid isolation of genomic DNA from Gram-negative bacteria. . Trends Genet 8:, 332–333.[PubMed] [CrossRef]
    [Google Scholar]
  21. Ogasawara H. , Hasegawa A. , Kanda E. , Miki T. , Yamamoto K. Y. , Ishihama A. . ( 2007; ). Genomic SELEX search for target promoters under the control of the PhoQP-RstBA signal relay cascade. . J Bacteriol 189:, 4791–4799. [CrossRef] [PubMed]
    [Google Scholar]
  22. Ogasawara H. , Yamamoto K. , Ishihama A. . ( 2010a; ). Regulatory role of MlrA in transcription activation of csgD, the master regulator of biofilm formation in Escherichia coli. . FEMS Microbiol Lett 312:, 160–168. [CrossRef] [PubMed]
    [Google Scholar]
  23. Ogasawara H. , Yamada K. , Kori A. , Yamamoto K. , Ishihama A. . ( 2010b; ). Regulation of the Escherichia coli csgD promoter: interplay between five transcription factors. . Microbiology 156:, 2470–2483. [CrossRef] [PubMed]
    [Google Scholar]
  24. Olsén A. , Arnqvist A. , Hammar M. , Sukupolvi S. , Normark S. . ( 1993; ). The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli . . Mol Microbiol 7:, 523–536. [CrossRef] [PubMed]
    [Google Scholar]
  25. Parker C. T. , Kyle J. L. , Huynh S. , Carter M. Q. , Brandl M. T. , Mandrell R. E. . ( 2012; ). Distinct transcriptional profiles and phenotypes exhibited by Escherichia coli O157:H7 isolates related to the 2006 spinach-associated outbreak. . Appl Environ Microbiol 78:, 455–463. [CrossRef] [PubMed]
    [Google Scholar]
  26. Pesavento C. , Becker G. , Sommerfeldt N. , Possling A. , Tschowri N. , Mehlis A. , Hengge R. . ( 2008; ). Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. . Genes Dev 22:, 2434–2446. [CrossRef] [PubMed]
    [Google Scholar]
  27. Robbe-Saule V. , Jaumouillé V. , Prévost M. C. , Guadagnini S. , Talhouarne C. , Mathout H. , Kolb A. , Norel F. . ( 2006; ). Crl activates transcription initiation of RpoS-regulated genes involved in the multicellular behavior of Salmonella enterica serovar Typhimurium. . J Bacteriol 188:, 3983–3994. [CrossRef] [PubMed]
    [Google Scholar]
  28. 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 Microbiol 67:, 4901–4907. [CrossRef] [PubMed]
    [Google Scholar]
  29. Rosser T. , Dransfield T. , Allison L. , Hanson M. , Holden N. , Evans J. , Naylor S. , La Ragione R. , Low J. C. , Gally D. L. . ( 2008; ). Pathogenic potential of emergent sorbitol-fermenting Escherichia coli O157:NM. . Infect Immun 76:, 5598–5607. [CrossRef] [PubMed]
    [Google Scholar]
  30. Shaikh N. , Tarr P. I. . ( 2003; ). Escherichia coli O157:H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. . J Bacteriol 185:, 3596–3605. [CrossRef] [PubMed]
    [Google Scholar]
  31. Sommerfeldt N. , Possling A. , Becker G. , Pesavento C. , Tschowri N. , Hengge R. . ( 2009; ). Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. . Microbiology 155:, 1318–1331. [CrossRef] [PubMed]
    [Google Scholar]
  32. Subbarayan P. R. , Sarkar M. . ( 2004a; ). A stop codon-dependent internal secondary translation initiation region in Escherichia coli rpoS. . RNA 10:, 1359–1365. [CrossRef] [PubMed]
    [Google Scholar]
  33. Subbarayan P. R. , Sarkar M. . ( 2004b; ). Escherichia coli rpoS gene has an internal secondary translation initiation region. . Biochem Biophys Res Commun 313:, 294–299. [CrossRef] [PubMed]
    [Google Scholar]
  34. Thomason M. K. , Storz G. . ( 2010; ). Bacterial antisense RNAs: how many are there, and what are they doing?. Annu Rev Genet 44:, 167–188. [CrossRef] [PubMed]
    [Google Scholar]
  35. Thomason M. K. , Fontaine F. , De Lay N. , Storz G. . ( 2012; ). A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli. . Mol Microbiol 84:, 17–35. [CrossRef] [PubMed]
    [Google Scholar]
  36. 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 Microbiol 67:, 2367–2370. [CrossRef] [PubMed]
    [Google Scholar]
  37. 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 Microbiol 72:, 2564–2572. [CrossRef] [PubMed]
    [Google Scholar]
  38. Uhlich G. A. , Sinclair J. R. , Warren N. G. , Chmielecki W. A. , Fratamico P. . ( 2008; ). Characterization of Shiga toxin-producing Escherichia coli isolates associated with two multistate food-borne outbreaks that occurred in 2006. . Appl Environ Microbiol 74:, 1268–1272. [CrossRef] [PubMed]
    [Google Scholar]
  39. Uhlich G. A. , Chen C. Y. , Cottrell B. J. , Irwin P. L. , Phillips J. G. . ( 2012; ). Peroxide resistance in Escherichia coli serotype O157 : H7 biofilms is regulated by both RpoS-dependent and -independent mechanisms. . Microbiology 158:, 2225–2234. [CrossRef] [PubMed]
    [Google Scholar]
  40. Van Houdt R. , Michiels C. W. . ( 2005; ). Role of bacterial cell surface structures in Escherichia coli biofilm formation. . Res Microbiol 156:, 626–633. [CrossRef] [PubMed]
    [Google Scholar]
  41. Vidal O. , Longin R. , Prigent-Combaret C. , Dorel C. , Hooreman M. , Lejeune P. . ( 1998; ). Isolation of an Escherichia coli K-12 mutant strain able to form biofilms on inert surfaces: involvement of a new ompR allele that increases curli expression. . J Bacteriol 180:, 2442–2449.[PubMed]
    [Google Scholar]
  42. 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 Immun 64:, 2808–2811.[PubMed]
    [Google Scholar]
  43. Weber H. , Pesavento C. , Possling A. , Tischendorf G. , Hengge R. . ( 2006; ). Cyclic-di-GMP-mediated signalling within the σs network of Escherichia coli . . Mol Microbiol 62:, 1014–1034. [CrossRef] [PubMed]
    [Google Scholar]
  44. Zambrano M. M. , Siegele D. A. , Almirón M. , Tormo A. , Kolter R. . ( 1993; ). Microbial competition: Escherichia coli mutants that take over stationary phase cultures. . Science 259:, 1757–1760. [CrossRef] [PubMed]
    [Google Scholar]
  45. Zheng D. , Constantinidou C. , Hobman J. L. , Minchin S. D. . ( 2004; ). Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. . Nucleic Acids Res 32:, 5874–5893. [CrossRef] [PubMed]
    [Google Scholar]
  46. Zogaj X. , Nimtz M. , Rohde M. , Bokranz W. , Römling U. . ( 2001; ). The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. . Mol Microbiol 39:, 1452–1463. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.066118-0
Loading
/content/journal/micro/10.1099/mic.0.066118-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error