Advertisement

Transcriptional Regulation Between the Two Global Regulators RovA and CRP in Yersinia pestis biovar Microtus

  • Lei Liu
  • Haihong Fang
  • Yinjuan Ding
  • Yaqiong Zheng
  • Liping Cai
  • Shangen Zheng
  • Yiquan Zhang
Article

Abstract

Yersinia pestis is a dangerous bacterial pathogen that can cause plague. Both RovA and cyclic AMP receptor protein (cAMP-CRP) are required for regulating biofilm- and virulence-related genes in Y. pestis. In this study, the transcriptional regulation between RovA and cAMP-CRP were analyzed by using primer extension, quantitative RT-PCR, LacZ fusion, and electrophoretic mobility shift assay. The results indicated that RovA repressed crp transcription in an indirect manner, while that RovA had no regulatory action on cyaA at the transcriptional level. In addition, cAMP-CRP did not regulate the transcription of rovA. Taken together with our previous results, complex regulatory interactions of RovA, cAMP-CRP, and PhoP/PhoQ in Y. pestis were revealed, which would promote us gain deeper understanding about coordinative modulation of biofilm- and virulence-related regulator genes.

Notes

Acknowledgements

This work was supported by the National Natural Science Foundation of China (81801984), and by the Natural Science Foundation of Hubei Province (2018CFB184), and by the Hubei Province health and family planning scientific research project (WJ2018H0070).

Supplementary material

284_2018_1571_MOESM1_ESM.docx (426 kb)
Supplementary material 1 (DOCX 425 KB)

References

  1. 1.
    Zhou D, Yang R (2011) Formation and regulation of Yersinia biofilms. Protein Cell 2:173–179CrossRefGoogle Scholar
  2. 2.
    Han Y, Qiu J, Guo Z, Gao H, Song Y, Zhou D, Yang R (2007) Comparative transcriptomics in Yersinia pestis: a global view of environmental modulation of gene expression. BMC Microbiol 7:96CrossRefGoogle Scholar
  3. 3.
    Cathelyn JS, Crosby SD, Lathem WW, Goldman WE, Miller VL (2006) RovA, a global regulator of Yersinia pestis, specifically required for bubonic plague. Proc Natl Acad Sci USA 103:13514–13519CrossRefGoogle Scholar
  4. 4.
    Dube PH, Handley SA, Revell PA, Miller VL (2003) The rovA mutant of Yersinia enterocolitica displays differential degrees of virulence depending on the route of infection. Infect Immun 71:3512–3520CrossRefGoogle Scholar
  5. 5.
    Nagel G, Heroven AK, Eitel J, Dersch P (2003) Function and regulation of the transcriptional activator RovA of Yersinia pseudotuberculosis. Adv Exp Med Biol 529:285–287CrossRefGoogle Scholar
  6. 6.
    Derbise A, Chenal-Francisque V, Pouillot F, Fayolle C, Prevost MC, Medigue C, Hinnebusch BJ, Carniel E (2007) A horizontally acquired filamentous phage contributes to the pathogenicity of the plague bacillus. Mol Microbiol 63:1145–1157CrossRefGoogle Scholar
  7. 7.
    Zhang Y, Wang L, Fang N, Qu S, Tan Y, Guo Z, Qiu J, Zhou D, Yang R (2013) Reciprocal regulation of pH 6 antigen gene loci by PhoP and RovA in Yersinia pestis biovar Microtus. Future Microbiol 8:271–280CrossRefGoogle Scholar
  8. 8.
    Liu L, Fang H, Yang H, Zhang Y, Han Y, Zhou D, Yang R (2016) Reciprocal regulation of Yersinia pestis biofilm formation and virulence by RovM and RovA. Open Biol 6:150198CrossRefGoogle Scholar
  9. 9.
    Heroven AK, Dersch P (2006) RovM, a novel LysR-type regulator of the virulence activator gene rovA, controls cell invasion, virulence and motility of Yersinia pseudotuberculosis. Mol Microbiol 62:1469–1483CrossRefGoogle Scholar
  10. 10.
    Zhan L, Han Y, Yang L, Geng J, Li Y, Gao H, Guo Z, Fan W, Li G, Zhang L et al (2008) 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 76:5028–5037CrossRefGoogle Scholar
  11. 11.
    Oh MH, Lee SM, Lee DH, Choi SH (2009) Regulation of the Vibrio vulnificus hupA gene by temperature alteration and cyclic AMP receptor protein and evaluation of its role in virulence. Infect Immun 77:1208–1215CrossRefGoogle Scholar
  12. 12.
    Petersen S, Young GM (2002) Essential role for cyclic AMP and its receptor protein in Yersinia enterocolitica virulence. Infect Immun 70:3665–3672CrossRefGoogle Scholar
  13. 13.
    Rickman L, Scott C, Hunt DM, Hutchinson T, Menendez MC, Whalan R, Hinds J, Colston MJ, Green J, Buxton RS (2005) A member of the cAMP receptor protein family of transcription regulators in Mycobacterium tuberculosis is required for virulence in mice and controls transcription of the rpfA gene coding for a resuscitation promoting factor. Mol Microbiol 56:1274–1286CrossRefGoogle Scholar
  14. 14.
    Skorupski K, Taylor RK (1997) Cyclic AMP and its receptor protein negatively regulate the coordinate expression of cholera toxin and toxin-coregulated pilus in Vibrio cholerae. Proc Natl Acad Sci USA 94:265–270CrossRefGoogle Scholar
  15. 15.
    Busby S, Ebright RH (1999) Transcription activation by catabolite activator protein (CAP). J Mol Biol 293:199–213CrossRefGoogle Scholar
  16. 16.
    Kim TJ, Chauhan S, Motin VL, Goh EB, Igo MM, Young GM (2007) Direct transcriptional control of the plasminogen activator gene of Yersinia pestis by the cyclic AMP receptor protein. J Bacteriol 189:8890–8900CrossRefGoogle Scholar
  17. 17.
    Liu H, Wang H, Qiu J, Wang X, Guo Z, Qiu Y, Zhou D, Han Y, Du Z, Li C et al (2009) Transcriptional profiling of a mice plague model: insights into interaction between Yersinia pestis and its host. J Basic Microbiol 49:92–99CrossRefGoogle Scholar
  18. 18.
    Zhan L, Yang L, Zhou L, Li Y, Gao H, Guo Z, Zhang L, Qin C, Zhou D, Yang R (2009) Direct and negative regulation of the sycO-ypkA-ypoJ operon by cyclic AMP receptor protein (CRP) in Yersinia pestis. BMC Microbiol 9:178CrossRefGoogle Scholar
  19. 19.
    Willias SP, Chauhan S, Lo CC, Chain PS, Motin VL (2015) CRP-mediated carbon catabolite regulation of Yersinia pestis biofilm formation is enhanced by the carbon storage regulator protein, CsrA. PLoS ONE 10:e0135481CrossRefGoogle Scholar
  20. 20.
    Liu L, Fang H, Yang H, Zhang Y, Han Y, Zhou D, Yang R (2016) CRP is an activator of Yersinia pestis biofilm formation that operates via a mechanism involving gmhA and waaAE-coaD. Front Microbiol 7:295PubMedPubMedCentralGoogle Scholar
  21. 21.
    Groisman EA (2001) The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183:1835–1842CrossRefGoogle Scholar
  22. 22.
    Rebeil R, Jarrett CO, Driver JD, Ernst RK, Oyston PC, Hinnebusch BJ (2013) Induction of the Yersinia pestis PhoP-PhoQ regulatory system in the flea and its role in producing a transmissible infection. J Bacteriol 195:1920–1930CrossRefGoogle Scholar
  23. 23.
    Vadyvaloo V, Viall AK, Jarrett CO, Hinz AK, Sturdevant DE, Hinnebusch J, B (2015) Role of the PhoP-PhoQ gene regulatory system in adaptation of Yersinia pestis to environmental stress in the flea digestive tract. Microbiology 161:1198–1210CrossRefGoogle Scholar
  24. 24.
    Liu L, Fang N, Sun Y, Yang H, Zhang Y, Han Y, Zhou D, Yang R (2014) Transcriptional regulation of the waaAE-coaD operon by PhoP and RcsAB in Yersinia pestis biovar Microtus. Protein Cell 5:940–944CrossRefGoogle Scholar
  25. 25.
    Oyston PC, Dorrell N, Williams K, Li SR, Green M, Titball RW, Wren BW (2000) The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect Immun 68:3419–3425CrossRefGoogle Scholar
  26. 26.
    Grabenstein JP, Fukuto HS, Palmer LE, Bliska JB (2006) Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect Immun 74:3727–3741CrossRefGoogle Scholar
  27. 27.
    Bozue J, Mou S, Moody KL, Cote CK, Trevino S, Fritz D, Worsham P (2011) The role of the phoPQ operon in the pathogenesis of the fully virulent CO92 strain of Yersinia pestis and the IP32953 strain of Yersinia pseudotuberculosis. Microb Pathog 50:314–321CrossRefGoogle Scholar
  28. 28.
    Zhang Y, Wang L, Han Y, Yan Y, Tan Y, Zhou L, Cui Y, Du Z, Wang X, Bi Y et al (2013) Autoregulation of PhoP/PhoQ and positive regulation of the cyclic AMP receptor protein-cyclic AMP complex by PhoP in Yersinia pestis. J Bacteriol 195:1022–1030CrossRefGoogle Scholar
  29. 29.
    Zhang Y, Gao H, Wang L, Xiao X, Tan Y, Guo Z, Zhou D, Yang R (2011) Molecular characterization of transcriptional regulation of rovA by PhoP and RovA in Yersinia pestis. PLoS ONE 6:e25484CrossRefGoogle Scholar
  30. 30.
    Zhou D, Tong Z, Song Y, Han Y, Pei D, Pang X, Zhai J, Li M, Cui B, Qi Z et al (2004) Genetics of metabolic variations between Yersinia pestis biovars and the proposal of a new biovar, microtus. J Bacteriol 186:5147–5152CrossRefGoogle Scholar
  31. 31.
    Sun F, Gao H, Zhang Y, Wang L, Fang N, Tan Y, Guo Z, Xia P, Zhou D, Yang R (2012) Fur is a repressor of biofilm formation in Yersinia pestis. PLoS ONE 7:e52392CrossRefGoogle Scholar
  32. 32.
    Sun F, Zhang Y, Qiu Y, Yang H, Yang W, Yin Z, Wang J, Yang R, Xia P, Zhou D (2014) H-NS is a repressor of major virulence gene loci in Vibrio parahaemolyticus. Front Microbiol 5:675PubMedPubMedCentralGoogle Scholar
  33. 33.
    El-Robh MS, Busby SJ (2002) The Escherichia coli cAMP receptor protein bound at a single target can activate transcription initiation at divergent promoters: a systematic study that exploits new promoter probe plasmids. Biochem J 368:835–843CrossRefGoogle Scholar
  34. 34.
    Liu Z, Gao X, Wang H, Fang H, Yan Y, Liu L, Chen R, Zhou D, Yang R, Han Y (2016) Plasmid pPCP1-derived sRNA HmsA promotes biofilm formation of Yersinia pestis. BMC Microbiol 16:176CrossRefGoogle Scholar
  35. 35.
    Fang N, Qu S, Yang H, Fang H, Liu L, Zhang Y, Wang L, Han Y, Zhou D, Yang R (2014) HmsB enhances biofilm formation in Yersinia pestis. Front Microbiol 5:685CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of TransfusionWuhan General Hospital of PLAWuhanChina
  2. 2.State Key Laboratory of Pathogen and BiosecurityBeijing Institute of Microbiology and EpidemiologyBeijingChina
  3. 3.School of MedicineJiangsu UniversityZhenjiangChina

Personalised recommendations