Advertisement

Current Microbiology

, Volume 75, Issue 6, pp 773–778 | Cite as

Reciprocal Regulation of OmpR and Hfq and Their Regulatory Actions on the Vi Polysaccharide Capsular Antigen in Salmonella enterica Serovar Typhi

  • Ying Zhang
  • Lin Xia
  • Liping Lin
  • Hao Tang
  • George Osei-Adjei
  • Shungao Xu
  • Yiquan ZhangEmail author
  • Xinxiang HuangEmail author
Article

Abstract

Salmonella enterica serovar Typhi (S. Typhi) is the causative agent of human typhoid fever. S. Typhi expresses a major virulence determinant called Vi polysaccharide capsular antigen, which is encoded by the viaB locus containing 10 consecutive genes including tviA and tviB. Expression of Vi antigen is regulated by the two-component regulatory system EnvZ/OmpR and the global RNA-binding factor Hfq. In this study, we show that OmpR coordinates with Hfq to regulate the transcription of Vi antigen genes under osmotic stress conditions. OmpR binds to the promoters of tviA and its own genes to activate their transcription; however, it positively regulates tviB and negatively regulates hfq in an indirect manner. Moreover, Hfq reversely inhibits ompR, tviA and tviB, and positively regulates its own gene expression. Thus, we report of a complex gene regulatory network involving the reciprocal regulation and autoregulation of OmpR and Hfq, and their regulatory actions on Vi polysaccharide capsular antigen genes in S. Typhi.

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31400125), Professional Research Foundation for Advanced Talents of Jiangsu University (13JDG026), Natural Science Fund for Colleges and Universities in Jiangsu Province (14KJB180005).

Compliance with Ethical Standards

Conflict of interest

The authors declare that there is no competing interest.

Supplementary material

284_2018_1447_MOESM1_ESM.jpg (51 kb)
Supplementary Fig. S1 Gene regulatory network. The arrow line represents positive regulation. The vertical lines represents negative regulation. (JPG 50 KB)
284_2018_1447_MOESM2_ESM.jpg (823 kb)
Supplementary Fig. S2 Structural organization of target promoters. The DNA sequence was derived from S. Typhi GIFU 10007. The transcription start sites of tviA [16] and ompR [26] are indicated by bent arrows. Shine-Dalgarno (SD) sequence, -10 and -35 elements were enclosed in boxes. The putative OmpR sites were underlined with solid lines. (JPG 822 KB)

References

  1. 1.
    Crump JA, Sjolund-Karlsson M, Gordon MA, Parry CM (2015) Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections. Clin Microbiol Rev 28(4):901–937.  https://doi.org/10.1128/Cmr.00002-15 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Hashimoto Y, Li N, Yokoyama H, Ezaki T (1993) Complete nucleotide sequence and molecular characterization of ViaB region encoding Vi antigen in Salmonella typhi. J Bacteriol 175(14):4456–4465CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Pickard D, Wain J, Baker S, Line A, Chohan S, Fookes M, Barron A, Gaora PO, Chabalgoity JA, Thanky N, Scholes C, Thomson N, Quail M, Parkhill J, Dougan G (2003) Composition, acquisition, and distribution of the Vi exopolysaccharide-encoding Salmonella enterica pathogenicity island SPI-7. J Bacteriol 185(17):5055–5065CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Santander J, Roland KL, Curtiss R 3rd (2008) Regulation of Vi capsular polysaccharide synthesis in Salmonella enterica serotype Typhi. J Infect Dev Ctries 2 (6):412–420PubMedPubMedCentralGoogle Scholar
  5. 5.
    Looney RJ, Steigbigel RT (1986) Role of the Vi antigen of Salmonella typhi in resistance to host defense in vitro. J Lab Clin Med 108(5):506–516PubMedGoogle Scholar
  6. 6.
    Wilson RP, Winter SE, Spees AM, Winter MG, Nishimori JH, Sanchez JF, Nuccio SP, Crawford RW, Tukel C, Baumler AJ (2011) The Vi capsular polysaccharide prevents complement receptor 3-mediated clearance of Salmonella enterica serotype Typhi. Infect Immun 79(2):830–837.  https://doi.org/10.1128/IAI.00961-10 CrossRefPubMedGoogle Scholar
  7. 7.
    Wangdi T, Lee CY, Spees AM, Yu C, Kingsbury DD, Winter SE, Hastey CJ, Wilson RP, Heinrich V, Baumler AJ (2014) The Vi capsular polysaccharide enables Salmonella enterica serovar typhi to evade microbe-guided neutrophil chemotaxis. PLoS Pathog 10(8):e1004306.  https://doi.org/10.1371/journal.ppat.1004306 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Wilson RP, Raffatellu M, Chessa D, Winter SE, Tukel C, Baumler AJ (2008) The Vi-capsule prevents Toll-like receptor 4 recognition of Salmonella. Cell Microbiol 10(4):876–890.  https://doi.org/10.1111/j.1462-5822.2007.01090.x CrossRefPubMedGoogle Scholar
  9. 9.
    Raffatellu M, Chessa D, Wilson RP, Dusold R, Rubino S, Baumler AJ (2005) The Vi capsular antigen of Salmonella enterica serotype Typhi reduces Toll-like receptor-dependent interleukin-8 expression in the intestinal mucosa. Infect Immun 73(6):3367–3374.  https://doi.org/10.1128/IAI.73.6.3367-3374.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Waxin H, Virlogeux I, Kolyva S, Popoff MY (1993) Identification of six open reading frames in the Salmonella enterica subsp. enterica ser. Typhi viaB locus involved in Vi antigen production. Res Microbiol 144(5):363–371  https://doi.org/10.1016/0923-2508(93)90193-6 CrossRefPubMedGoogle Scholar
  11. 11.
    Janis C, Grant AJ, McKinley TJ, Morgan FJ, John VF, Houghton J, Kingsley RA, Dougan G, Mastroeni P (2011) In vivo regulation of the Vi antigen in Salmonella and induction of immune responses with an in vivo-inducible promoter. Infect Immun 79(6):2481–2488.  https://doi.org/10.1128/IAI.01265-10 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Tran QT, Gomez G, Khare S, Lawhon SD, Raffatellu M, Bäumler AJ, Ajithdoss D, Dhavala S, Adams LG (2010) The Salmonella enterica serotype Typhi Vi capsular antigen is expressed after the bacterium enters the ileal mucosa. Infect Immun 78(1):527–535.  https://doi.org/10.1128/IAI.00972-09 CrossRefPubMedGoogle Scholar
  13. 13.
    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(7):3084–3089PubMedPubMedCentralGoogle Scholar
  14. 14.
    Arricau N, Hermant D, Waxin H, Ecobichon C, Duffey PS, Popoff MY (1998) The RcsB-RcsC regulatory system of Salmonella typhi differentially modulates the expression of invasion proteins, flagellin and Vi antigen in response to osmolarity. Mol Microbiol 29(3):835–850CrossRefPubMedGoogle Scholar
  15. 15.
    Pickard D, Li J, Roberts M, Maskell D, Hone D, Levine M, Dougan G, Chatfield S (1994) Characterization of defined ompR mutants of Salmonella typhi: ompR is involved in the regulation of Vi polysaccharide expression. Infect Immun 62(9):3984–3993PubMedPubMedCentralGoogle Scholar
  16. 16.
    Virlogeux I, Waxin H, Ecobichon C, Lee JO, Popoff MY (1996) Characterization of the rcsA and rcsB genes from Salmonella typhi: rcsB through tviA is involved in regulation of Vi antigen synthesis. J Bacteriol 178(6):1691–1698CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Wehland M, Bernhard F (2000) The RcsAB box. Characterization of a new operator essential for the regulation of exopolysaccharide biosynthesis in enteric bacteria. J Biol Chem 275(10):7013–7020.  https://doi.org/10.1074/jbc.275.10.7013 CrossRefPubMedGoogle Scholar
  18. 18.
    Hashimoto Y, Khan AQ, Ezaki T (1996) Positive autoregulation of vipR expression in ViaB region-encoded Vi antigen of Salmonella typhi. J Bacteriol 178(5):1430–1436CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Perkins TT, Davies MR, Klemm EJ, Rowley G, Wileman T, James K, Keane T, Maskell D, Hinton JC, Dougan G, Kingsley RA (2013) ChIP-seq and transcriptome analysis of the OmpR regulon of Salmonella enterica serovars Typhi and Typhimurium reveals accessory genes implicated in host colonization. Mol Microbiol 87(3):526–538.  https://doi.org/10.1111/mmi.12111 CrossRefPubMedGoogle Scholar
  20. 20.
    Xie X, Li A, Du H, Sheng X, Zhang H, Xu S, Huang X (2010) Expression of tviA is transiently repressed by Hfq in Salmonella enterica serovar Typhi at hyperosmotic stress. Microb Pathog 49(1–2):54–57.  https://doi.org/10.1016/j.micpath.2010.03.011 CrossRefPubMedGoogle Scholar
  21. 21.
    Xu S, Zou X, Sheng X, Zhang H, Mao L, Du H, Xu H, Huang X (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 41(3):729–740.  https://doi.org/10.1590/S1517-83822010000300025 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Gao H, Zhang Y, Yang L, Liu X, Guo Z, Tan Y, Han Y, Huang X, Zhou D, Yang R (2011) Regulatory effects of cAMP receptor protein (CRP) on porin genes and its own gene in Yersinia pestis. BMC Microbiol 11:40.  https://doi.org/10.1186/1471-2180-11-40 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Gao H, Zhang Y, Han Y, Yang L, Liu X, Guo Z, Tan Y, Huang X, Zhou D, Yang R (2011) Phenotypic and transcriptional analysis of the osmotic regulator OmpR in Yersinia pestis. BMC Microbiol 11:39.  https://doi.org/10.1186/1471-2180-11-39 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Gao H, Zhang L, Osei-Adjei G, Yang W, Zhou D, Huang X, Yang H, Yin Z, Zhang Y (2017) Transcriptional regulation of cpsQ-mfpABC and mfpABC by CalR in Vibrio parahaemolyticus. Microbiologyopen 6 (4).  https://doi.org/10.1002/mbo3.470
  25. 25.
    Zhang L, Osei-Adjei G, Zhang Y, Gao H, Yang W, Zhou D, Huang X, Yang H (2017) CalR is required for the expression of T6SS2 and the adhesion of Vibrio parahaemolyticus to HeLa cells. Arch Microbiol 199(6):931–938.  https://doi.org/10.1007/s00203-017-1361-6 CrossRefPubMedGoogle Scholar
  26. 26.
    Bang IS, Audia JP, Park YK, Foster JW (2002) Autoinduction of the ompR response regulator by acid shock and control of the Salmonella enterica acid tolerance response. Mol Microbiol 44(5):1235–1250.  https://doi.org/10.1046/j.1365-2958.2002.02937.x CrossRefPubMedGoogle Scholar
  27. 27.
    van Helden J (2003) Regulatory sequence analysis tools. Nucleic Acids Res 31(13):3593–3596CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Pruss BM (2017) Involvement of two-component signaling on bacterial motility and biofilm development. J Bacteriol.  https://doi.org/10.1128/JB.00259-17 PubMedPubMedCentralGoogle Scholar
  29. 29.
    Wang LC, Morgan LK, Godakumbura P, Kenney LJ, Anand GS (2012) The inner membrane histidine kinase EnvZ senses osmolality via helix-coil transitions in the cytoplasm. EMBO J 31(11):2648–2659.  https://doi.org/10.1038/emboj.2012.99 CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Flores-Valdez MA, Fernandez-Mora M, Ares MA, Giron JA, Calva E, De la Cruz MA (2014) OmpR phosphorylation regulates ompS1 expression by differentially controlling the use of promoters. Microbiology 160(Pt 4):733–741.  https://doi.org/10.1099/mic.0.071381-0 CrossRefPubMedGoogle Scholar
  31. 31.
    De la Cruz MA, Calva E (2010) The complexities of porin genetic regulation. J Mol Microbiol Biotechnol 18(1):24–36.  https://doi.org/10.1159/000274309 CrossRefPubMedGoogle Scholar
  32. 32.
    Samanta P, Clark ER, Knutson K, Horne SM, Pruss BM (2013) OmpR and RcsB abolish temporal and spatial changes in expression of flhD in Escherichia coli biofilm. BMC Microbiol 13:182.  https://doi.org/10.1186/1471-2180-13-182 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Schwan WR, Lee JL, Lenard FA, Matthews BT, Beck MT (2002) Osmolarity and pH growth conditions regulate fim gene transcription and type 1 pilus expression in uropathogenic Escherichia coli. Infect Immun 70(3):1391–1402.  https://doi.org/10.1128/IAI.70.3.1391-1402.2002 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Rentschler AE, Lovrich SD, Fitton R, Enos-Berlage J, Schwan WR (2013) OmpR regulation of the uropathogenic Escherichia coli fimB gene in an acidic/high osmolality environment. Microbiology 159(Pt 2):316–327.  https://doi.org/10.1099/mic.0.059386-0 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Prigent-Combaret C, Brombacher E, Vidal O, Ambert A, Lejeune P, Landini P, Dorel C (2001) Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 183(24):7213–7223.  https://doi.org/10.1128/JB.183.24.7213-7223.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Ishihama A (2000) Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol 54:499–518.  https://doi.org/10.1146/annurev.micro.54.1.499 CrossRefPubMedGoogle Scholar
  37. 37.
    Sharma AK, Payne SM (2006) Induction of expression of hfq by DksA is essential for Shigella flexneri virulence. Mol Microbiol 62(2):469–479.  https://doi.org/10.1111/j.1365-2958.2006.05376.x CrossRefPubMedGoogle Scholar
  38. 38.
    Sobrero P, Valverde C (2011) Evidences of autoregulation of hfq expression in Sinorhizobium meliloti strain 2011. Arch Microbiol 193(9):629–639.  https://doi.org/10.1007/s00203-011-0701-1 CrossRefPubMedGoogle Scholar
  39. 39.
    Vogel J, Luisi BF (2011) Hfq and its constellation of RNA. Nat Rev Microbiol 9(8):578–589.  https://doi.org/10.1038/nrmicro2615 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Kakoschke T, Kakoschke S, Magistro G, Schubert S, Borath M, Heesemann J, Rossier O (2014) The RNA chaperone Hfq impacts growth, metabolism and production of virulence factors in Yersinia enterocolitica. PLoS ONE 9(1):e86113.  https://doi.org/10.1371/journal.pone.0086113 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Kulesus RR, Diaz-Perez K, Slechta ES, Eto DS, Mulvey MA (2008) Impact of the RNA chaperone Hfq on the fitness and virulence potential of uropathogenic Escherichia coli. Infect Immun 76(7):3019–3026.  https://doi.org/10.1128/IAI.00022-08 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Ying Zhang
    • 1
  • Lin Xia
    • 2
  • Liping Lin
    • 1
  • Hao Tang
    • 1
  • George Osei-Adjei
    • 1
  • Shungao Xu
    • 1
  • Yiquan Zhang
    • 1
    Email author
  • Xinxiang Huang
    • 1
    Email author
  1. 1.School of MedicineJiangsu UniversityZhenjiangChina
  2. 2.Department of Clinical Laboratory, Affiliated HospitalJiangsu UniversityZhenjiangChina

Personalised recommendations