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.

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2013-07-01
2019-12-06
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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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
  14. Ishikawa S.. ( 1991;). [The role of fimbriae of Escherichia coli in urinary tract infections]. . Hinyokika Kiyo 37:, 953–956 [in Japanese].[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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
  18. Jonas K., Melefors O., Römling U.. ( 2009;). Regulation of c-di-GMP metabolism in biofilms. . Future Microbiol 4:, 341–358. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
  30. Römling U.. ( 2009;). Rationalizing the evolution of EAL domain-based cyclic di-GMP-specific phosphodiesterases. . J Bacteriol 191:, 4697–4700. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
  33. Schwan W. R.. ( 2011;). Regulation of fim genes in uropathogenic Escherichia coli.. World J Clin Infect Dis 1:, 17–25. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
  36. Skorupski K., Taylor R. K.. ( 1996;). Positive selection vectors for allelic exchange. . Gene 169:, 47–52. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][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. [CrossRef][PubMed]
    [Google Scholar]
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