1887

Abstract

In serovar Typhimurium, the RcsCDB regulatory system controls the expression of genes involved in synthesis of colanic acid, formation of flagella and virulence. Here, we show that activation of the RcsCDB system downregulates expression of an operon that encodes fimbriae involved in attachment to the mucus layer in the large intestine. Bioinformatic analysis predicts the existence of an RcsB-binding site located 180 bp upstream to the +1 transcription start site of the promoter, and electrophoretic mobility shift assays confirm that RcsB binds the promoter region . This study adds RcsB to the list of regulators of transcription and provides an example of modulation of fimbriae synthesis by a signal transduction system.

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/content/journal/micro/10.1099/mic.0.000854
2019-11-01
2019-12-06
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References

  1. Winfield MD, Groisman EA. Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl Environ Microbiol 2003;69:3687–3694 [CrossRef]
    [Google Scholar]
  2. Groisman EA, Mouslim C. Sensing by bacterial regulatory systems in host and non-host environments. Nat Rev Microbiol 2006;4:705–709 [CrossRef]
    [Google Scholar]
  3. Coburn B, Grassl GA, Salmonella FBB. The host and disease: a brief review. Immunol Cell Biol 2007;85:112–118
    [Google Scholar]
  4. Beier D, Gross R. Regulation of bacterial virulence by two-component systems. Curr Opin Microbiol 2006;9:143–152 [CrossRef]
    [Google Scholar]
  5. Kato A, Groisman EA. Howard Hughes Medical Institute The PhoQ/PhoP regulatory network of Salmonella enterica. Adv Exp Med Biol 2008;631:7–21 [CrossRef]
    [Google Scholar]
  6. Majdalani N, Gottesman S. The RCS phosphorelay: a complex signal transduction system. Annu Rev Microbiol 2005;59:379–405 [CrossRef]
    [Google Scholar]
  7. Clarke DJ. The RCS phosphorelay: more than just a two-component pathway. Future Microbiol 2010;5:1173–1184 [CrossRef]
    [Google Scholar]
  8. Guo XP, Sun YC. New insights into the Non-orthodox two component RCS phosphorelay system. Front Microbiol 2014;2017:8
    [Google Scholar]
  9. Domínguez-Bernal G, Pucciarelli MG, Ramos-Morales F, García-Quintanilla M, Cano DA et al. Repression of the RcsC-YojN-RcsB phosphorelay by the IgaA protein is a requisite for Salmonella virulence. Mol Microbiol 2004;53:1437–1449 [CrossRef]
    [Google Scholar]
  10. Mouslim C, Delgado M, Groisman EA. Activation of the RcsC/YojN/RcsB phosphorelay system attenuates Salmonella virulence. Mol Microbiol 2004;54:386–395 [CrossRef]
    [Google Scholar]
  11. García-Calderón CB, García-Quintanilla M, Casadesús J, Ramos-Morales F. Virulence attenuation in Salmonella enterica rcsC mutants with constitutive activation of the RCS system. Microbiology 2005;151:579–588 [CrossRef]
    [Google Scholar]
  12. Delgado MA, Mouslim C, Groisman EA. The PmrA/PmrB and RcsC/YojN/RcsB systems control expression of the Salmonella O-antigen chain length determinant. Mol Microbiol 2006;60:39–50 [CrossRef]
    [Google Scholar]
  13. Farizano JV, Torres MA, Pescaretti MdeLM, Delgado MA. The RcsCDB regulatory system plays a crucial role in the protection of Salmonella enterica serovar Typhimurium against oxidative stress. Microbiology 2014;160:2190–2199 [CrossRef]
    [Google Scholar]
  14. Torrez Lamberti MF, Farizano JV, López FE, Martínez Zamora MG, Pescaretti MM et al. Cross-talk between the RcsCDB and RstAB systems to control STM1485 gene expression in Salmonella Typhimurium during acid-resistance response. Biochimie 2019;160:46–54 [CrossRef]
    [Google Scholar]
  15. Humphries AD, Townsend SM, Kingsley RA, Nicholson TL, Tsolis RM et al. Role of fimbriae as antigens and intestinal colonization factors of Salmonella serovars. FEMS Microbiol Lett 2001;201:121–125 [CrossRef]
    [Google Scholar]
  16. Nuccio S-P, Bäumler AJ. Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev 2007;71:551–575 [CrossRef]
    [Google Scholar]
  17. Yue M, Rankin SC, Blanchet RT, Nulton JD, Edwards RA et al. Diversification of the Salmonella fimbriae: a model of macro- and microevolution. PLoS One 2012;7:e38596 [CrossRef]
    [Google Scholar]
  18. Chessa D, Winter MG, Jakomin M, Bäumler AJ. Salmonella enterica serotype Typhimurium Std fimbriae bind terminal α(1,2)fucose residues in the cecal mucosa. Mol Microbiol 2009;71:864–875 [CrossRef]
    [Google Scholar]
  19. García-Pastor L, Sánchez-Romero MA, Gutiérrez G, Puerta-Fernández E, Casadesús J. Formation of phenotypic lineages in Salmonella enterica by a pleiotropic fimbrial switch. PLoS Genet 2018;14:e1007677 [CrossRef]
    [Google Scholar]
  20. Humphries AD, Raffatellu M, Winter S, Weening EH, Kingsley RA et al. The use of flow cytometry to detect expression of subunits encoded by 11 Salmonella enterica serotype Typhimurium fimbrial operons. Mol Microbiol 2003;48:1357–1376 [CrossRef]
    [Google Scholar]
  21. Jakomin M, Chessa D, Bäumler AJ, Casadesús J. Regulation of the Salmonella enterica STD fimbrial operon by DNA adenine methylation, SeqA, and HdfR. J Bacteriol 2008;190:7406–7413 [CrossRef]
    [Google Scholar]
  22. Suwandi A, Galeev A, Riedel R, Sharma S, Seeger K et al. Std fimbriae-fucose interaction increases Salmonella-induced intestinal inflammation and prolongs colonization. PLoS Pathog 2019;15:e1007915 [CrossRef]
    [Google Scholar]
  23. López-Garrido J, Casadesús J. Crosstalk between virulence loci: regulation of Salmonella enterica pathogenicity island 1 (SPI-1) by products of the std fimbrial operon. PLoS One 2012;7:e30499 [CrossRef]
    [Google Scholar]
  24. García-Pastor L, Sánchez-Romero MA, Jakomin M, Puerta-Fernández E, Casadesús J. Regulation of bistability in the std fimbrial operon of Salmonella enterica by DNA adenine methylation and transcription factors HdfR, StdE and StdF. Nucleic Acids Res 2019;36: [CrossRef]
    [Google Scholar]
  25. Davis RW, Botstein D, Roth JR. Advanced Bacterial Genetics Cold Spring Harbor, New York: Cold Spring Harbor Laboratory; 1980
    [Google Scholar]
  26. Pescaretti MdeLM, Morero R, Delgado MA. Identification of a new promoter for the response regulator rcsB expression in Salmonella enterica serovar Typhimurium. FEMS Microbiol Lett 2009;300:165–173 [CrossRef]
    [Google Scholar]
  27. Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: A Laboratory Manual Cold Spring Harbor, New York: Cold Spring Harbor Laboratory; 1989
    [Google Scholar]
  28. Miller JH. Experiments in molecular genetics. cold Spring Harbor, N. Y.: Cold Spring Harbor Laboratory 1972;xvi466
    [Google Scholar]
  29. Lehti TA, Heikkinen J, Korhonen TK, Westerlund-Wikström B. The response regulator RcsB activates expression of Mat fimbriae in meningitic Escherichia coli. J Bacteriol 2012;194:3475–3485 [CrossRef]
    [Google Scholar]
  30. Costa CS, Antón DN. Role of the ftsA1p promoter in the resistance of mucoid mutants of Salmonella enterica to mecillinam: characterization of a new type of mucoid mutant. FEMS Microbiol Lett 2001;200:201–205 [CrossRef]
    [Google Scholar]
  31. Hu LI, Chi BK, Kuhn ML, Filippova EV, Walker-Peddakotla AJ et al. Acetylation of the response regulator RcsB controls transcription from a small RNA promoter. J Bacteriol 2013;195:4174–4186 [CrossRef]
    [Google Scholar]
  32. Bailey TL, Elkan C. The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 1995;3:21–29
    [Google Scholar]
  33. Bailey TL, Gribskov M. Methods and statistics for combining motif match scores. J Comput Biol 1998;5:211–221 [CrossRef]
    [Google Scholar]
  34. Carballès F, Bertrand C, Bouché JP, Cam K. Regulation of Escherichia coli cell division genes ftsA and ftsZ by the two-component system rcsC-rcsB. Mol Microbiol 1999;34:442–450 [CrossRef]
    [Google Scholar]
  35. Wehland M, Bernhard F. The RcsAB box. Characterization of a new operator essential for the regulation of exopolysaccharide biosynthesis in enteric bacteria. J Biol Chem 2000;275:7013–7020 [CrossRef]
    [Google Scholar]
  36. Mouslim C, Latifi T, Groisman EA. Signal-Dependent requirement for the co-activator protein RcsA in transcription of the RcsB-regulated ugd gene. J Biol Chem 2003;278:50588–50595 [CrossRef]
    [Google Scholar]
  37. Hernday AD, Braaten BA, Broitman-Maduro G, Engelberts P, Low DA. Regulation of the pap epigenetic switch by CpxAR: phosphorylated CpxR inhibits transition to the phase on state by competition with Lrp. Mol Cell 2004;16:537–547 [CrossRef]
    [Google Scholar]
  38. Weyand NJ, Braaten BA, van der Woude M, Tucker J, Low DA. The essential role of the promoter-proximal subunit of cap in pap phase variation: Lrp- and helical phase-dependent activation of papBA transcription by cap from -215. Mol Microbiol 2001;39:1504–1522 [CrossRef]
    [Google Scholar]
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