1887

Abstract

CG43, a heavy encapsulated liver abscess isolate, mainly expresses type 3 fimbriae. Type 1 fimbriae expression was only apparent in CG43S3Δ (the type 3 fimbriae-deficient strain). The expression of type 1 fimbriae in CG43S3Δ was reduced by deleting the gene, but was unaffected by removing the 3′ end of encoding the C-terminal EIL domain (EIL). Quantitative RT-PCR and promoter activity analysis showed that the putative DNA-binding region at the N terminus, but not the C-terminal EIL domain, of FimK positively affects transcription of the type 1 fimbrial major subunit, . An electrophoretic mobility shift assay demonstrated that the recombinant FimK could specifically bind to , which is located upstream of and contains a vegetative promoter for the operon, also reflecting possible transcriptional regulation. EIL was shown to encode a functional phosphodiesterase (PDE) via enhancing motility in JM109 and using PDE activity assays. Moreover, EIL exhibited higher PDE activity than FimK, implying that the N-terminal DNA-binding domain may negatively affect the PDE activity of FimK. FimA expression was detected in CG43S3 expressing EIL or AIL, suggesting that FimA expression is not directly influenced by the c-di-GMP level. In summary, FimK influences type 1 fimbriation by binding to at the N-terminal domain, and thereafter, the altered protein structure may activate C-terminal PDE activity to reduce the intracellular c-di-GMP level.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.067793-0
2013-07-01
2021-08-04
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/7/1402.html?itemId=/content/journal/micro/10.1099/mic.0.067793-0&mimeType=html&fmt=ahah

References

  1. Bassis C. M., Visick K. L.( 2010). The cyclic-di-GMP phosphodiesterase BinA negatively regulates cellulose-containing biofilms in Vibrio fischeri. J Bacteriol 192:1269–1278 [View Article][PubMed]
    [Google Scholar]
  2. Blumer C., Kleefeld A., Lehnen D., Heintz M., Dobrindt U., Nagy G., Michaelis K., Emödy L., Polen T. et al.( 2005). Regulation of type 1 fimbriae synthesis and biofilm formation by the transcriptional regulator LrhA of Escherichia coli. Microbiology 151:3287–3298 [View Article][PubMed]
    [Google Scholar]
  3. Chang H. Y., Lee J. H., Deng W. L., Fu T. F., Peng H. L.( 1996). Virulence and outer membrane properties of a galU mutant of Klebsiella pneumoniae CG43. Microb Pathog 20:255–261 [View Article][PubMed]
    [Google Scholar]
  4. Christen M., Christen B., Folcher M., Schauerte A., Jenal U.( 2005). Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J Biol Chem 280:30829–30837 [View Article][PubMed]
    [Google Scholar]
  5. Chuang Y. P., Fang C. T., Lai S. Y., Chang S. C., Wang J. T.( 2006). Genetic determinants of capsular serotype K1 of Klebsiella pneumoniae causing primary pyogenic liver abscess. J Infect Dis 193:645–654 [View Article][PubMed]
    [Google Scholar]
  6. Cruz D. P., Huertas M. G., Lozano M., Zárate L., Zambrano M. M.( 2012). Comparative analysis of diguanylate cyclase and phosphodiesterase genes in Klebsiella pneumoniae. BMC Microbiol 12:139 [View Article][PubMed]
    [Google Scholar]
  7. Eisenstein B. I., Sweet D. S., Vaughn V., Friedman D. I.( 1987). Integration host factor is required for the DNA inversion that controls phase variation in Escherichia coli. Proc Natl Acad Sci U S A 84:6506–6510 [View Article][PubMed]
    [Google Scholar]
  8. Fung C. P., Chang F. Y., Lee S. C., Hu B. S., Kuo B. I. T., Liu C. Y., Ho M., Siu L. K.( 2002). A global emerging disease of Klebsiella pneumoniae liver abscess: is serotype K1 an important factor for complicated endophthalmitis?. Gut 50:420–424 [View Article][PubMed]
    [Google Scholar]
  9. Galperin M. Y., Nikolskaya A. N., Koonin E. V.( 2001). Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203:11–21 [View Article][PubMed]
    [Google Scholar]
  10. Guzman L. M., Belin D., Carson M. J., Beckwith J.( 1995). Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121–4130[PubMed]
    [Google Scholar]
  11. Han S. H. B.( 1995). Review of hepatic abscess from Klebsiella pneumoniae. An association with diabetes mellitus and septic endophthalmitis. West J Med 162:220–224[PubMed]
    [Google Scholar]
  12. Ho Y. S. J., Burden L. M., Hurley J. H.( 2000). Structure of the GAF domain, a ubiquitous signaling motif and a new class of cyclic GMP receptor. EMBO J 19:5288–5299 [View Article][PubMed]
    [Google Scholar]
  13. Huang Y. J., Liao H. W., Wu C. C., Peng H. L.( 2009). MrkF is a component of type 3 fimbriae in Klebsiella pneumoniae. Res Microbiol 160:71–79 [View Article][PubMed]
    [Google Scholar]
  14. Ishikawa S.( 1991). [The role of fimbriae of Escherichia coli in urinary tract infections]. Hinyokika Kiyo 37:953–956[PubMed]
    [Google Scholar]
  15. Johnson J. G., Clegg S.( 2010). Role of MrkJ, a phosphodiesterase, in type 3 fimbrial expression and biofilm formation in Klebsiella pneumoniae. J Bacteriol 192:3944–3950 [View Article][PubMed]
    [Google Scholar]
  16. Johnson J. G., Murphy C. N., Sippy J., Johnson T. J., Clegg S.( 2011). Type 3 fimbriae and biofilm formation are regulated by the transcriptional regulators MrkHI in Klebsiella pneumoniae. J Bacteriol 193:3453–3460 [View Article][PubMed]
    [Google Scholar]
  17. Jonas K., Edwards A. N., Simm R., Romeo T., Römling U., Melefors O.( 2008). The RNA binding protein CsrA controls cyclic di-GMP metabolism by directly regulating the expression of GGDEF proteins. Mol Microbiol 70:236–257 [View Article][PubMed]
    [Google Scholar]
  18. Jonas K., Melefors O., Römling U.( 2009). Regulation of c-di-GMP metabolism in biofilms. Future Microbiol 4:341–358 [View Article][PubMed]
    [Google Scholar]
  19. Jones C. H., Pinkner J. S., Roth R., Heuser J., Nicholes A. V., Abraham S. N., Hultgren S. J.( 1995). FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae. Proc Natl Acad Sci U S A 92:2081–2085 [View Article][PubMed]
    [Google Scholar]
  20. Jones C. H., Danese P. N., Pinkner J. S., Silhavy T. J., Hultgren S. J.( 1997). The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J 16:6394–6406 [View Article][PubMed]
    [Google Scholar]
  21. Keen N. T., Tamaki S., Kobayashi D., Trollinger D.( 1988). Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70:191–197 [View Article][PubMed]
    [Google Scholar]
  22. Kuchma S. L., Brothers K. M., Merritt J. H., Liberati N. T., Ausubel F. M., O’Toole G. A.( 2007). BifA, a cyclic-di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189:8165–8178 [View Article][PubMed]
    [Google Scholar]
  23. Lai Y. C., Peng H. L., Chang H. Y.( 2003). RmpA2, an activator of capsule biosynthesis in Klebsiella pneumoniae CG43, regulates K2 cps gene expression at the transcriptional level. J Bacteriol 185:788–800 [View Article][PubMed]
    [Google Scholar]
  24. Lin C. T., Huang Y. J., Chu P. H., Hsu J. L., Huang C. H., Peng H. L.( 2006). Identification of an HptB-mediated multi-step phosphorelay in Pseudomonas aeruginosa PAO1. Res Microbiol 157:169–175 [View Article][PubMed]
    [Google Scholar]
  25. McFarland K. A., Lucchini S., Hinton J. C. D., Dorman C. J.( 2008). The leucine-responsive regulatory protein, Lrp, activates transcription of the fim operon in Salmonella enterica serovar typhimurium via the fimZ regulatory gene. J Bacteriol 190:602–612 [View Article][PubMed]
    [Google Scholar]
  26. Otto K., Norbeck J., Larsson T., Karlsson K. A., Hermansson M.( 2001). Adhesion of type 1-fimbriated Escherichia coli to abiotic surfaces leads to altered composition of outer membrane proteins. J Bacteriol 183:2445–2453 [View Article][PubMed]
    [Google Scholar]
  27. Pope J. V., Teich D. L., Clardy P., McGillicuddy D. C.( 2011). Klebsiella pneumoniae liver abscess: an emerging problem in North America. J Emerg Med 41:e103–e105 [View Article][PubMed]
    [Google Scholar]
  28. Rao F., Yang Y., Qi Y. N., Liang Z. X.( 2008). Catalytic mechanism of cyclic di-GMP-specific phosphodiesterase: a study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J Bacteriol 190:3622–3631 [View Article][PubMed]
    [Google Scholar]
  29. Rao F., Qi Y. N., Chong H. S., Kotaka M., Li B., Li J. M., Lescar J., Tang K., Liang Z. X.( 2009). The functional role of a conserved loop in EAL domain-based cyclic di-GMP-specific phosphodiesterase. J Bacteriol 191:4722–4731 [View Article][PubMed]
    [Google Scholar]
  30. Römling U.( 2009). Rationalizing the evolution of EAL domain-based cyclic di-GMP-specific phosphodiesterases. J Bacteriol 191:4697–4700 [View Article][PubMed]
    [Google Scholar]
  31. Rosen D. A., Pinkner J. S., Jones J. M., Walker J. N., Clegg S., Hultgren S. J.( 2008). Utilization of an intracellular bacterial community pathway in Klebsiella pneumoniae urinary tract infection and the effects of FimK on type 1 pilus expression. Infect Immun 76:3337–3345 [View Article][PubMed]
    [Google Scholar]
  32. Schelenz S., Bramham K., Goldsmith D.( 2007). Septic arthritis due to extended spectrum beta lactamase producing Klebsiella pneumoniae. Joint Bone Spine 74:275–278 [View Article][PubMed]
    [Google Scholar]
  33. Schwan W. R.( 2011). Regulation of fim genes in uropathogenic Escherichia coli.. World J Clin Infect Dis 1:17–25 [View Article][PubMed]
    [Google Scholar]
  34. Simm R., Morr M., Kader A., Nimtz M., Römling U.( 2004). GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53:1123–1134 [View Article][PubMed]
    [Google Scholar]
  35. Sjöström A. E., Balsalobre C., Emödy L., Westerlund-Wikström B., Hacker J., Uhlin B. E.( 2009). The SfaXII protein from newborn meningitis E. coli is involved in regulation of motility and type 1 fimbriae expression. Microb Pathog 46:243–252 [View Article][PubMed]
    [Google Scholar]
  36. Skorupski K., Taylor R. K.( 1996). Positive selection vectors for allelic exchange. Gene 169:47–52 [View Article][PubMed]
    [Google Scholar]
  37. Snyder J. A., Haugen B. J., Lockatell C. V., Maroncle N., Hagan E. C., Johnson D. E., Welch R. A., Mobley H. L. T.( 2005). Coordinate expression of fimbriae in uropathogenic Escherichia coli. Infect Immun 73:7588–7596 [View Article][PubMed]
    [Google Scholar]
  38. Stahlhut S. G., Struve C., Krogfelt K. A., Reisner A.( 2012). Biofilm formation of Klebsiella pneumoniae on urethral catheters requires either type 1 or type 3 fimbriae. FEMS Immunol Med Microbiol 65:350–359 [View Article][PubMed]
    [Google Scholar]
  39. Struve C., Bojer M., Krogfelt K. A.( 2008). Characterization of Klebsiella pneumoniae type 1 fimbriae by detection of phase variation during colonization and infection and impact on virulence. Infect Immun 76:4055–4065 [View Article][PubMed]
    [Google Scholar]
  40. Struve C., Bojer M., Krogfelt K. A.( 2009). Identification of a conserved chromosomal region encoding Klebsiella pneumoniae type 1 and type 3 fimbriae and assessment of the role of fimbriae in pathogenicity. Infect Immun 77:5016–5024 [View Article][PubMed]
    [Google Scholar]
  41. Tamayo R., Pratt J. T., Camilli A.( 2007). Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61:131–148 [View Article][PubMed]
    [Google Scholar]
  42. Tang H. L., Chiang M. K., Liou W. J., Chen Y. T., Peng H. L., Chiou C. S., Liu K. S., Lu M. C., Tung K. C., Lai Y. C.( 2010). Correlation between Klebsiella pneumoniae carrying pLVPK-derived loci and abscess formation. Eur J Clin Microbiol Infect Dis 29:689–698 [View Article][PubMed]
    [Google Scholar]
  43. Teng C. H., Xie Y., Shin S., Di Cello F., Paul-Satyaseela M., Cai M., Kim K. S.( 2006). Effects of ompA deletion on expression of type 1 fimbriae in Escherichia coli K1 strain RS218 and on the association of E. coli with human brain microvascular endothelial cells. Infect Immun 74:5609–5616 [View Article][PubMed]
    [Google Scholar]
  44. Tsai K. W., Lai H. T., Tsai T. C., Wu Y. C., Yang Y. T., Chen K. Y., Chen C. M., Li Y. S. J., Chen C. N.( 2009). Difference in the regulation of IL-8 expression induced by uropathogenic E. coli between two kinds of urinary tract epithelial cells. J Biomed Sci 16:91 [View Article][PubMed]
    [Google Scholar]
  45. Wilksch J. J., Yang J., Clements A., Gabbe J. L., Short K. R., Cao H. W., Cavaliere R., James C. E., Whitchurch C. B. et al.( 2011). MrkH, a novel c-di-GMP-dependent transcriptional activator, controls Klebsiella pneumoniae biofilm formation by regulating type 3 fimbriae expression. PLoS Pathog 7:e1002204 [View Article][PubMed]
    [Google Scholar]
  46. Wood T. K., González Barrios A. F., Herzberg M., Lee J.( 2006). Motility influences biofilm architecture in Escherichia coli. Appl Microbiol Biotechnol 72:361–367 [View Article][PubMed]
    [Google Scholar]
  47. Wu C. C., Huang Y. J., Fung C. P., Peng H. L.( 2010). Regulation of the Klebsiella pneumoniae Kpc fimbriae by the site-specific recombinase KpcI. Microbiology 156:1983–1992 [View Article][PubMed]
    [Google Scholar]
  48. Xia Y., Gally D., Forsman-Semb K., Uhlin B. E.( 2000). Regulatory cross-talk between adhesin operons in Escherichia coli: inhibition of type 1 fimbriae expression by the PapB protein. EMBO J 19:1450–1457 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.067793-0
Loading
/content/journal/micro/10.1099/mic.0.067793-0
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