1887

Abstract

The serovar Typhi genome contains 14 putative fimbrial systems. The Std fimbriae belong to the chaperone-usher family and its regulation has not been investigated in . Typhi. Several regulators of Std were previously identified in the closely related serovar Typhimurium. We hypothesize that regulators of . Typhimurium may be shared with . Typhi, but that several other regulators remain to be discovered. Here, we describe the role of more than 50 different candidate regulators on expression. Three types of regulators were investigated: known regulators in . Typhimurium, predicted regulators and virulence/metabolic regulators. Expression of was determined in the regulator mutants and compared with the wild-type strain. Overall, 21 regulator mutations affect promoter expression. The role of Crp, a newly identified factor for expression, was further investigated. Crp acted as an activator of expression on a distal region of the promoter region. Together, our results demonstrate the major influence of Crp as a novel transcriptional factor on promoter expression and later production of Std fimbriae in .

Keyword(s): Crp , fimbriae , promoter , regulation and Std
Funding
This study was supported by the:
  • Natural Sciences and Engineering Research Council of Canada (Award RGPIN-2020-05233)
    • Principle Award Recipient: FranceDaigle
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001022
2021-01-21
2024-10-09
Loading full text...

Full text loading...

/deliver/fulltext/micro/167/3/micro001022.html?itemId=/content/journal/micro/10.1099/mic.0.001022&mimeType=html&fmt=ahah

References

  1. Nuccio S-P, Bäumler AJ. Evolution of the chaperone/usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev 2007; 71:551–575 [View Article][PubMed]
    [Google Scholar]
  2. Dufresne K, Saulnier-Bellemare J, Daigle F. Functional Analysis of the Chaperone-Usher Fimbrial Gene Clusters of Salmonella enterica serovar Typhi. Front Cell Infect Microbiol 2018; 8:26 [View Article][PubMed]
    [Google Scholar]
  3. 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 [View Article][PubMed]
    [Google Scholar]
  4. Chessa D, Winter MG, Jakomin M, Bäumler AJ. Salmonella enterica serotype Typhimurium Std fimbriae bind terminal alpha(1,2)fucose residues in the cecal mucosa. Mol Microbiol 2009; 71:864–875 [View Article][PubMed]
    [Google Scholar]
  5. 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 [View Article][PubMed]
    [Google Scholar]
  6. 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 [View Article][PubMed]
    [Google Scholar]
  7. 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; 47:7929–7941 [View Article][PubMed]
    [Google Scholar]
  8. 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 [View Article][PubMed]
    [Google Scholar]
  9. Chessa D, Winter MG, Nuccio S-P, Tükel C, Bäumler AJ. RosE represses Std fimbrial expression in Salmonella enterica serotype Typhimurium. Mol Microbiol 2008; 68:573–587 [View Article][PubMed]
    [Google Scholar]
  10. Andrews-Polymenis H, Bäumler AJ. Pathogenomics of Salmonella species. In Hacker K, Dobrindt U. (editors) Pathogenomics Weinheim: Wiley; 2006 pp 109–124
    [Google Scholar]
  11. Leclerc J-M, Dozois CM, Daigle F. Role of the Salmonella enterica serovar Typhi Fur regulator and small RNAs RfrA and RfrB in iron homeostasis and interaction with host cells. Microbiology 2013; 159:591–602 [View Article][PubMed]
    [Google Scholar]
  12. O'Callaghan D, Charbit A. High efficiency transformation of Salmonella typhimurium and Salmonella typhi by electroporation. Mol Gen Genet 1990; 223:156–158 [View Article][PubMed]
    [Google Scholar]
  13. Forest C, Faucher SP, Poirier K, Houle S, Dozois CM et al. Contribution of the stg fimbrial operon of Salmonella enterica serovar Typhi during interaction with human cells. Infect Immun 2007; 75:5264–5271 [View Article][PubMed]
    [Google Scholar]
  14. Miller JH. Experiments in molecular genetics. In Harbor CS. editor NY: Cold Spring Harbor Laboratory; 1972
  15. Simons RW, Houman F, Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 1987; 53:85–96 [View Article][PubMed]
    [Google Scholar]
  16. Hone DM, Harris AM, Chatfield S, Dougan G, Levine MM. Construction of genetically defined double aro mutants of Salmonella typhi. Vaccine 1991; 9:810–816 [View Article][PubMed]
    [Google Scholar]
  17. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 2001; 413:848–852 [View Article][PubMed]
    [Google Scholar]
  18. Murret-Labarthe C, Kerhoas M, Dufresne K, Daigle F. New roles for two-component system response Regulators of Salmonella enterica serovar Ttyphi during host cell Interactions. Microorganisms 2020; 8:e722 13 05 2020 [View Article][PubMed]
    [Google Scholar]
  19. Jofré MR, Rodríguez LM, Villagra NA, Hidalgo AA, Mora GC et al. RpoS integrates CRP, Fis, and PhoP signaling pathways to control Salmonella Typhi hlyE expression. BMC Microbiol 2014; 14:139 [View Article][PubMed]
    [Google Scholar]
  20. Zhan L, Han Y, Yang L, Geng J, Li Y et al. The cyclic AMP receptor protein, CRP, is required for both virulence and expression of the minimal CRP regulon in Yersinia pestis biovar microtus. Infect Immun 2008; 76:5028–5037 [View Article][PubMed]
    [Google Scholar]
  21. Fuentes JA, Jofré MR, Villagra NA, Mora GC. RpoS- and Crp-dependent transcriptional control of Salmonella typhi taiA and hlyE genes: role of environmental conditions. Res Microbiol 2009; 160:800–808 [View Article][PubMed]
    [Google Scholar]
  22. Tsai Y-L, Chien H-F, Huang K-T, Lin W-Y, Liaw S-J. cAMP receptor protein regulates mouse colonization, motility, fimbria-mediated adhesion, and stress tolerance in uropathogenic Proteus mirabilis . Sci Rep 2017; 7:7282 [View Article][PubMed]
    [Google Scholar]
  23. Kalivoda EJ, Stella NA, O'Dee DM, Nau GJ, Shanks RMQ. The cyclic AMP-dependent catabolite repression system of Serratia marcescens mediates biofilm formation through regulation of type 1 fimbriae. Appl Environ Microbiol 2008; 74:3461–3470 [View Article][PubMed]
    [Google Scholar]
  24. Lin C-T, Lin T-H, Wu C-C, Wan L, Huang C-F et al. CRP-Cyclic AMP Regulates the Expression of Type 3 Fimbriae via Cyclic di-GMP in Klebsiella pneumoniae . PLoS One 2016; 11:e0162884 [View Article][PubMed]
    [Google Scholar]
  25. Müller CM, Aberg A, Straseviçiene J, Emody L, Uhlin BE et al. Type 1 fimbriae, a colonization factor of uropathogenic Escherichia coli, are controlled by the metabolic sensor CRP-cAMP. PLoS Pathog 2009; 5:e1000303 [View Article][PubMed]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.001022
Loading
/content/journal/micro/10.1099/mic.0.001022
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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