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RpoE may Promote Flagellar Gene Expression in Salmonella enterica Serovar Typhi Under Hyperosmotic Stress

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Abstract

Salmonella enterica serovar Typhi z66 positive strain contains a fljBA-like operon on a linear plasmid. The operon contains the gene fljB:z66 which encodes the z66 antigen. RpoE is a sigma factor σE that initiates transcription of a series of genes in Escherichia and Salmonella under environmental stresses. To investigate whether the gene fljB:z66 is regulated by RpoE (σE), a rpoE deletion mutant of S. enterica serovar Typhi (ΔrpoE) was prepared in this study. The defective motility of the ΔrpoE was confirmed firstly. Transcriptional expression of flagellar genes was screened using a genomic DNA microarray. Some class-2 and most class-3 flagellar genes were downregulated in the ΔrpoE after 30 min of hyperosmotic stress. The expression of fliA and fljB:z66, a class-2 flagellar gene and a class-3 flagellar gene, obviously decreased; however, expression of the class-1 flagellar genes flhDC did not change obviously in the ΔrpoE compared to the wild-type strain in the same conditions. Results of quantitative real-time PCR (qRT-PCR) showed that the expression levels of fliA and fljB:z66 in the ΔrpoE after 30 min of hyperosmotic stress decreased about five and eightfold, respectively, compared to the wild-type strain. Similar results were observed at 120 min of hyperosmotic stress. Western blotting and qRT-PCR analysis showed that expression of fliA and fljB:z66 was significantly increased after supplemental expression of rpoE with a recombinant plasmid pBADrpoE in the ΔrpoE strain. These results demonstrated that RpoE promoted the expression of class-3 flagellar genes and it might be performed by initiating the expression of fliA in S. enterica serovar Typhi under hyperosmotic stress.

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References

  1. Alba BM, Gross CA (2004) Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol Microbiol 52:613–619

    Article  CAS  PubMed  Google Scholar 

  2. Alba BM, Leeds JA, Onufryk C et al (2002) DegS and YaeL participate sequentially in the cleavage of RseA to activate the sigma(E)-dependent extracytoplasmic stress response. Genes Dev 16:2156–2168

    Article  CAS  PubMed  Google Scholar 

  3. Alba BM, Zhong HJ, Pelayo JC, Gross CA (2001) degS (hhoB) is an essential Escherichia coli gene whose indispensable function is to provide sigma (E) activity. Mol Microbiol 40:1323–1333

    Article  CAS  PubMed  Google Scholar 

  4. Baker S, Hardy J, Sanderson KE et al (2007) A novel linear plasmid mediates flagellar variation in Salmonella Typhi. PLoS Pathog 3:e59

    Article  PubMed  Google Scholar 

  5. Baker S, Holt K, Whitehead S et al (2007) A linear plasmid truncation induces unidirectional flagellar phase change in H:z66 positive Salmonella Typhi. Mol Microbiol 66:1207–1218

    Article  CAS  PubMed  Google Scholar 

  6. Everest P, Wain J, Roberts M et al (2001) The molecular mechanisms of severe typhoid fever. Trends Microbiol 9:316–320

    Article  CAS  PubMed  Google Scholar 

  7. Frankel G, Newton SM, Schoolnik GK, Stocker BA (1989) Intragenic recombination in a flagellin gene: characterization of the H1-j gene of Salmonella typhi. EMBO J 8:3149–3152

    CAS  PubMed  Google Scholar 

  8. Grigorova IL, Chaba R, Zhong HJ et al (2004) Fine-tuning of the Escherichia coli sigmaE envelope stress response relies on multiple mechanisms to inhibit signal-independent proteolysis of the transmembrane anti-sigma factor, RseA. Genes Dev 18:2686–2697

    Article  CAS  PubMed  Google Scholar 

  9. Hayden JD, Ades SE (2008) The extracytoplasmic stress factor, sigmaE, is required to maintain cell envelope integrity in Escherichia coli. PLoS ONE 3:e1573

    Article  PubMed  Google Scholar 

  10. Huang X, Phung le V, Dejsirilert S et al (2004) Cloning and characterization of the gene encoding the z66 antigen of Salmonella enterica serovar Typhi. FEMS Microbiol Lett 234:239–246

    Article  CAS  PubMed  Google Scholar 

  11. Huang X, Xu H, Sun X et al (2007) Genome-wide scan of the gene expression kinetics of Salmonella enterica serovar Typhi during hyperosmotic stress. Int J Mol Sci 8:116–135

    Article  CAS  Google Scholar 

  12. Jones BD, Lee CA, Falkow S (1992) Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect Immun 60:2475–2480

    CAS  PubMed  Google Scholar 

  13. Kutsukake K, Iino T (1994) Role of the FliA-FlgM regulatory system on the transcriptional control of the flagellar regulon and flagellar formation in Salmonella typhimurium. J Bacteriol 176:3598–3605

    CAS  PubMed  Google Scholar 

  14. Kutsukake K, Ohya Y, Iino T (1990) Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J Bacteriol 172:741–747

    CAS  PubMed  Google Scholar 

  15. Leclerc GJ, Tartera C, Metcalf ES (1998) Environmental regulation of Salmonella typhi invasion-defective mutants. Infect Immun 66:682–691

    CAS  PubMed  Google Scholar 

  16. Liu SL, Ezaki T, Miura H et al (1988) Intact motility as a Salmonella typhi invasion-related factor. Infect Immun 56:1967–1973

    CAS  PubMed  Google Scholar 

  17. Mashimo T, Hashimoto M, Yamaguchi S, Aizawa S (2007) Temperature-hypersensitive sites of the flagellar switch component FliG in Salmonella enterica serovar typhimurium. J Bacteriol 189:5153–5160

    Article  CAS  PubMed  Google Scholar 

  18. Miticka H, Rowley G, Rezuchova B et al (2003) Transcriptional analysis of the rpoE gene encoding extracytoplasmic stress response sigma factor sigmaE in Salmonella enterica serovar Typhimurium. FEMS Microbiol Lett 226:307–314

    Article  CAS  PubMed  Google Scholar 

  19. Pickard D, Li J, Roberts M et al (1994) Characterization of defined ompR mutants of Salmonella typhi: ompR is involved in the regulation of Vi polysaccharide expression. Infect Immun 62:3984–3993

    CAS  PubMed  Google Scholar 

  20. Rhodius VA, Suh WC, Nonaka G et al (2006) Conserved and variable functions of the sigmaE stress response in related genomes. PLoS Biol 4:e2

    Article  PubMed  Google Scholar 

  21. Rolhion N, Carvalho FA, Darfeuille-Michaud A (2007) OmpC and the sigma(E) regulatory pathway are involved in adhesion and invasion of the Crohn’s disease-associated Escherichia coli strain LF82. Mol Microbiol 63:1684–1700

    Article  CAS  PubMed  Google Scholar 

  22. Sheng X, Huang X, Mao L et al (2009) Preparation of Salmonella enterica serovar Typhi genomic DNA microarrays for gene expression profiling analysis. Prog Biochem Biophys 36:306–312

    Google Scholar 

  23. Shin S, Park C (1995) Modulation of flagellar expression in Escherichia coli by acetyl phosphate and the osmoregulator OmpR. J Bacteriol 177:4696–4702

    CAS  PubMed  Google Scholar 

  24. Tartera C, Metcalf ES (1993) Osmolarity and growth phase overlap in regulation of Salmonella typhi adherence to and invasion of human intestinal cells. Infect Immun 61:3084–3089

    CAS  PubMed  Google Scholar 

  25. Testerman TL, Vazquez-Torres A, Xu Y et al (2002) The alternative sigma factor sigmaE controls antioxidant defences required for Salmonella virulence and stationary-phase survival. Mol Microbiol 43:771–782

    Article  CAS  PubMed  Google Scholar 

  26. Tusher V, Tibshirani R, Chu C (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5512

    Article  CAS  PubMed  Google Scholar 

  27. Wang Q, Suzuki A, Mariconda S et al (2005) Sensing wetness: a new role for the bacterial flagellum. EMBO J 24:2034–2042

    Article  CAS  PubMed  Google Scholar 

  28. Xu S, Zou X, Sheng X et al (2010) Expression of fljB:z66 on a linear plasmid of Salmonella enterica serovar Typhi is dependent on FliA and FlhDC and regulated by OmpR. Braz J Microbiol (accepted)

  29. Zhang H, Sheng X, Xu S et al (2009) Global transcriptional response of Salmonella enterica serovar Typhi to anti-z66 antiserum. FEMS Microbiol Lett 298:51–55

    Article  CAS  PubMed  Google Scholar 

  30. Zou X, Huang X, Xu S et al (2009) Identification of a fljA gene on a linear plasmid as the repressor gene of fliC in Salmonella enterica serovar Typhi. Microbiol Immunol 53:191–197

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank T. Ezaki (Gifu University) for bacterial strains, anti-z66 antiserum, and continuous support. This study was supported by National Natural Science Foundation of China (30870095), National Special Scientific Program (2008ZX10004-009), Science Foundation of Jiangsu University for Advanced Scholars and Special Team Program of Jiangsu University (2008-018-02).

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Correspondence to Xinxiang Huang.

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Du, H., Sheng, X., Zhang, H. et al. RpoE may Promote Flagellar Gene Expression in Salmonella enterica Serovar Typhi Under Hyperosmotic Stress. Curr Microbiol 62, 492–500 (2011). https://doi.org/10.1007/s00284-010-9734-y

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  • DOI: https://doi.org/10.1007/s00284-010-9734-y

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