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Volume 161, Issue 12

PecS regulates the urate-responsive expression of type 1 fimbriae in CG43 Free

Abstract

In the CG43 genome, the divergently transcribed genes coding for PecS, the MarR-type transcription factor, and PecM, the drug metabolite transporter, are located between the type 1 and type 3 fimbrial gene clusters. The intergenic sequence between and contains three putative PecS binding sites and a CpxR box. Electrophoretic mobility shift assay revealed that the recombinant PecS and CpxR could specifically bind to the sequence, and the specific interaction of PecS and could be attenuated by urate. The expression of and was negatively regulated by CpxAR and PecS, and was inducible by exogenous urate in the absence of . Compared with CG43S3Δ, the derived mutants CG43S3ΔΔ and CG43S3ΔΔΔ exerted similar levels of sensitivity to HO or paraquat, but higher levels of mannose-sensitive yeast agglutination activity and FimA production. The promoter activity and transcript levels of in CG43S3Δ were also increased by deleting . However, no binding activity between PecS and the promoter could be observed. Nevertheless, PecS deletion could reduce the expression of the global regulator HNS and release the negative effect of HNS on FimA expression. In CG43S3Δ, the expression of FimA as well as PecS was inducible by urate, whilst urate-induced FimA expression was inhibited by the deletion of . Taken together, we propose that PecS indirectly and negatively regulates the expression of type 1 fimbriae, and the regulation is urate-inducible in the absence of CpxAR.

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© 2015 The Authors
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2015-12-01
2024-04-16
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References

  1. Airich L. G., Tsyrenzhapova I. S., Vorontsova O. V., Feofanov A. V., Doroshenko V. G., Mashko S. V. (2010). Membrane topology analysis of the Escherichia coli aromatic amino acid efflux protein YddGJ Mol Microbiol Biotechnol 19189–197 [View Article][PubMed]. [Google Scholar]
  2. Alamillo J. M., García-Olmedo F. (2001). Effects of urate, a natural inhibitor of peroxynitrite-mediated toxicity, in the response of Arabidopsis thaliana to the bacterial pathogen Pseudomonas syringae Plant J 25529–540 [View Article][PubMed]. [Google Scholar]
  3. Averyanov A. (2009). Oxidative burst and plant disease resistanceFront Biosci 1142–152.[CrossRef] [Google Scholar]
  4. 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 abscessJ Infect Dis 193645–654 [View Article][PubMed]. [Google Scholar]
  5. Corcoran C. P., Dorman C. J. (2009). DNA relaxation-dependent phase biasing of the fim genetic switch in Escherichia coli depends on the interplay of H-NS, IHF and LRPMol Microbiol 741071–1082 [View Article][PubMed]. [Google Scholar]
  6. Di Martino P., Cafferini N., Joly B., Darfeuille-Michaud A. (2003). Klebsiella pneumoniae type 3 pili facilitate adherence and biofilm formation on abiotic surfacesRes Microbiol 1549–16 [View Article][PubMed]. [Google Scholar]
  7. Donato G. M., Kawula T. H. (1999). Phenotypic analysis of random hns mutations differentiate DNA-binding activity from properties of fimA promoter inversion modulation and bacterial motilityJ Bacteriol 181941–948[PubMed]. [Google Scholar]
  8. Ellison D. W., Miller V. L. (2006). Regulation of virulence by members of the MarR/SlyA familyCurr Opin Microbiol 9153–159 [View Article][PubMed]. [Google Scholar]
  9. Fouts D. E., Tyler H. L., DeBoy R. T., Daugherty S., Ren Q., Badger J. H., Durkin A. S., Huot H., Shrivastava S., other authors. (2008). Complete genome sequence of the N2-fixing broad host range endophyte Klebsiella pneumoniae 342 and virulence predictions verified in micePLoS Genet 4e1000141 [View Article][PubMed]. [Google Scholar]
  10. Fung C. P., Chang F. Y., Lee S. C., Hu B. S., Kuo B. I., 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 50420–424 [View Article][PubMed]. [Google Scholar]
  11. Han S. H. (1995). Review of hepatic abscess from Klebsiella pneumoniae. An association with diabetes mellitus and septic endophthalmitisWest J Med 162220–224[PubMed]. [Google Scholar]
  12. Hommais F., Oger-Desfeux C., Van Gijsegem F., Castang S., Ligori S., Expert D., Nasser W., Reverchon S. (2008). PecS is a global regulator of the symptomatic phase in the phytopathogenic bacterium Erwinia chrysanthemi 3937J Bacteriol 1907508–7522 [View Article][PubMed]. [Google Scholar]
  13. Hornick D. B., Allen B. L., Horn M. A., Clegg S. (1992). Adherence to respiratory epithelia by recombinant Escherichia coli expressing Klebsiella pneumoniae type 3 fimbrial gene productsInfect Immun 601577–1588[PubMed]. [Google Scholar]
  14. Huang C. J., Wang Z. C., Huang H. Y., Huang H. D., Peng H. L. (2013a). YjcC, a c-di-GMP phosphodiesterase protein, regulates the oxidative stress response and virulence of Klebsiella pneumoniae CG43PLoS One 8e66740 [View Article][PubMed]. [Google Scholar]
  15. Huang H., Mackel B. J., Grove A. (2013b). Streptomyces coelicolor encodes a urate-responsive transcriptional regulator with homology to PecS from plant pathogensJ Bacteriol 1954954–4965 [View Article][PubMed]. [Google Scholar]
  16. Hunke S., Keller R., Müller V. S. (2012). Signal integration by the Cpx-envelope stress systemFEMS Microbiol Lett 32612–22 [View Article][PubMed]. [Google Scholar]
  17. Jagnow J., Clegg S. (2003). Klebsiella pneumoniae MrkD-mediated biofilm formation on extracellular matrix- and collagen-coated surfacesMicrobiology 1492397–2405 [View Article][PubMed]. [Google Scholar]
  18. Johnson J. G., Clegg S. (2010). Role of MrkJ, a phosphodiesterase, in type 3 fimbrial expression and biofilm formation in Klebsiella pneumoniae J Bacteriol 1923944–3950 [View Article][PubMed]. [Google Scholar]
  19. 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 levelJ Bacteriol 185788–800 [View Article][PubMed]. [Google Scholar]
  20. Liao Y. C., Huang T. W., Chen F. C., Charusanti P., Hong J. S., Chang H. Y., Tsai S. F., Palsson B. O., Hsiung C. A. (2011). An experimentally validated genome-scale metabolic reconstruction of Klebsiella pneumoniae MGH 78578, iYL1228J Bacteriol 1931710–1717 [View Article][PubMed]. [Google Scholar]
  21. 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 PAO1Res Microbiol 157169–175 [View Article][PubMed]. [Google Scholar]
  22. Liu J., Obi I. R., Thanikkal E. J., Kieselbach T., Francis M. S. (2011). Phosphorylated CpxR restricts production of the RovA global regulator in Yersinia pseudotuberculosis PLoS One 6e23314 [View Article][PubMed]. [Google Scholar]
  23. McClain M. S., Blomfield I. C., Eisenstein B. I. (1991). Roles of fimB and fimE in site-specific DNA inversion associated with phase variation of type 1 fimbriae in Escherichia coli J Bacteriol 1735308–5314[PubMed]. [Google Scholar]
  24. Mhedbi-Hajri N., Malfatti P., Pédron J., Gaubert S., Reverchon S., Van Gijsegem F. (2011). PecS is an important player in the regulatory network governing the coordinated expression of virulence genes during the interaction between Dickeya dadantii 3937 and plantsEnviron Microbiol 132901–2914 [View Article][PubMed]. [Google Scholar]
  25. Nuccio S. P., Bäumler A. J. (2007). Evolution of the chaperone/usher assembly pathway: fimbrial classification goes GreekMicrobiol Mol Biol Rev 71551–575 [View Article][PubMed]. [Google Scholar]
  26. O'Gara J. P., Dorman C. J. (2000). Effects of local transcription and H-NS on inversion of the fim switch of Escherichia coli Mol Microbiol 36457–466 [View Article][PubMed]. [Google Scholar]
  27. Perera I. C., Grove A. (2010). Urate is a ligand for the transcriptional regulator PecSJ Mol Biol 402539–551 [View Article][PubMed]. [Google Scholar]
  28. Perera I. C., Grove A. (2011). MarR homologs with urate-binding signatureProtein Sci 20621–629 [View Article][PubMed]. [Google Scholar]
  29. Pope J. V., Teich D. L., Clardy P., McGillicuddy D. C. (2011). Klebsiella pneumoniae liver abscess: an emerging problem in North AmericaJ Emerg Med 41e103–e105 [View Article][PubMed]. [Google Scholar]
  30. Praillet T., Reverchon S., Nasser W. (1997a). Mutual control of the PecS/PecM couple, two proteins regulating virulence-factor synthesis in Erwinia chrysanthemi Mol Microbiol 24803–814 [View Article][PubMed]. [Google Scholar]
  31. Praillet T., Reverchon S., Robert-Baudouy J., Nasser W. (1997b). The PecM protein is necessary for the DNA-binding capacity of the PecS repressor, one of the regulators of virulence-factor synthesis in Erwinia chrysanthemi FEMS Microbiol Lett 154265–270 [View Article][PubMed]. [Google Scholar]
  32. Reverchon S., Nasser W., Robert-Baudouy J. (1994). pecS: a locus controlling pectinase, cellulase and blue pigment production in Erwinia chrysanthemi Mol Microbiol 111127–1139 [View Article][PubMed]. [Google Scholar]
  33. Rouanet C., Nasser W. (2001). The PecM protein of the phytopathogenic bacterium Erwinia chrysanthemi, membrane topology and possible involvement in the efflux of the blue pigment indigoidineJ Mol Microbiol Biotechnol 3309–318[PubMed]. [Google Scholar]
  34. Schelenz S., Bramham K., Goldsmith D. (2007). Septic arthritis due to extended spectrum beta lactamase producing Klebsiella pneumoniaeJoint Bone Spine 74275–278 [View Article][PubMed]. [Google Scholar]
  35. Schroll C., Barken K. B., Krogfelt K. A., Struve C. (2010). Role of type 1 and type 3 fimbriae in Klebsiella pneumoniae biofilm formationBMC Microbiol 10179 [View Article][PubMed]. [Google Scholar]
  36. Skorupski K., Taylor R. K. (1996). Positive selection vectors for allelic exchangeGene 16947–52 [View Article][PubMed]. [Google Scholar]
  37. 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 fimbriaeFEMS Immunol Med Microbiol 65350–359 [View Article][PubMed]. [Google Scholar]
  38. 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 pathogenicityInfect Immun 775016–5024 [View Article][PubMed]. [Google Scholar]
  39. 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 formationEur J Clin Microbiol Infect Dis 29689–698 [View Article][PubMed]. [Google Scholar]
  40. Tarkkanen A. M., Virkola R., Clegg S., Korhonen T. K. (1997). Binding of the type 3 fimbriae of Klebsiella pneumoniae to human endothelial and urinary bladder cellsInfect Immun 651546–1549[PubMed]. [Google Scholar]
  41. Van Houdt R., Michiels C. W. (2005). Role of bacterial cell surface structures in Escherichia coli biofilm formationRes Microbiol 156626–633 [View Article][PubMed]. [Google Scholar]
  42. Vogt S. L., Raivio T. L. (2012). Just scratching the surface: an expanding view of the Cpx envelope stress responseFEMS Microbiol Lett 3262–11 [View Article][PubMed]. [Google Scholar]
  43. Wang Z. C., Huang C. J., Huang Y. J., Wu C. C., Peng H. L. (2013). FimK regulation on the expression of type 1 fimbriae in Klebsiella pneumoniae CG43S3Microbiology 1591402–1415 [View Article][PubMed]. [Google Scholar]
  44. Wilkinson S. P., Grove A. (2004). HucR, a novel uric acid-responsive member of the MarR family of transcriptional regulators from Deinococcus radiodurans J Biol Chem 27951442–51450 [View Article][PubMed]. [Google Scholar]
  45. Wilksch J. J., Yang J., Clements A., Gabbe J. L., Short K. R., Cao H., Cavaliere R., James C. E., Whitchurch C. B., other authors. (2011). MrkH, a novel c-di-GMP-dependent transcriptional activator, controls Klebsiella pneumoniae biofilm formation by regulating type 3 fimbriae expressionPLoS Pathog 7e1002204 [View Article][PubMed]. [Google Scholar]
  46. Wu K. M., Li L. H., Yan J. J., Tsao N., Liao T. L., Tsai H. C., Fung C. P., Chen H. J., Liu Y. M., other authors. (2009). Genome sequencing and comparative analysis of Klebsiella pneumoniae NTUH-K2044, a strain causing liver abscess and meningitisJ Bacteriol 1914492–4501 [View Article][PubMed]. [Google Scholar]
  47. Wu C. C., Lin C. T., Cheng W. Y., Huang C. J., Wang Z. C., Peng H. L. (2012). Fur-dependent MrkHI regulation of type 3 fimbriae in Klebsiella pneumoniae CG43Microbiology 1581045–1056 [View Article][PubMed]. [Google Scholar]
  48. Yamamoto K., Ishihama A. (2006). Characterization of copper-inducible promoters regulated by CpxA/CpxR in Escherichia coli Biosci Biotechnol Biochem 701688–1695 [View Article][PubMed]. [Google Scholar]
  49. Zakataeva N. P., Kutukova E. A., Gronskii˘ S. V., Troshin P. V., Livshits V. A., Aleshin V. V. (2006). [Export of metabolites by the proteins of the DMT and RhtB families and its possible role in intercellular communication]Mikrobiologiia 75509–520 (in Russian)[PubMed]. [Google Scholar]
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PecS regulates the urate-responsive expression of type 1 fimbriae in Klebsiella pneumoniae CG43
Microbiology 161, 2395 (2015); https://doi.org/10.1099/mic.0.000185
/content/journal/micro/10.1099/mic.0.000185
/content/journal/micro/10.1099/mic.0.000185
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