Skip to main content

Quorum sensing-1 signaling of N-hexanoyl-l-homoserine lactone contributes to virulence in avian pathogenic Escherichia coli

Abstract

Avian pathogenic E. coli (APEC) caused avian colibacillosis is mostly common in poultry industry worldwide. APEC virulence factors lead to pathogenesis and the quorum sensing (QS) system is actively involved in the regulation of these virulence factors. Signaling molecules in QS are known as autoinducers (AIs). In QS-1, E. coli encodes a single LuxR homolog, i.e., SdiA, but does not express the LuxI homolog, an acyl-homoserine lactone (AHL) synthase of producing AI-1. Avian pathogenic E. coli (APEC) regulates its virulence genes expression in response to exogenous AHLs, but regulatory mechanisms of AHL and QS-1 are still unknown. This study targeted the APEC CE129 isolate as the reference strain, and the Yersinia enterocolitica yenI gene was expressed into APEC CE129. CE129/pyenI was conferred the ability to produce AHL signal. The CE129 SdiA mutant strain with an in-frame sdiA (AHL receptor) gene deletion was constructed by a λRed recombination system, which lost the ability to sense AHL. The goal of this study was to explore the function of QS-1 upon virulence and elucidate the regulatory effect of QS-1/AHL signals in the APEC strain. Adherence and invasion assays revealed that QS-1 affected APEC adherence and survival ability. APEC biofilm formation was also suppressed under C6HSL. Interestingly, APEC exhibited different phenotypes of acid tolerance and flagella expression when compared to enterotoxigenic E. coli or enterohemorrhagic E. coli (ETEC and EHEC, respectively). These findings enhance our understanding of the QS mechanism.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Atkinson S, Chang CY, Sockett RE, Camara M, Williams P (2006) Quorum sensing in Yersinia enterocolitica controls swimming and swarming motility. J Bacteriol 188(4):1451–1461. https://doi.org/10.1128/JB.188.4.1451-1461.2006

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Boyen F, Eeckhaut V, Van Immerseel F, Pasmans F, Ducatelle R, Haesebrouck F (2009) Quorum sensing in veterinary pathogens: mechanisms, clinical importance and future perspectives. Vet Microbiol 135(3–4):187–195. https://doi.org/10.1016/j.vetmic.2008.12.025

    CAS  Article  PubMed  Google Scholar 

  3. Cui Z et al (2016) Autoinducer-2 of quorum sensing is involved in cell damage caused by avian pathogenic Escherichia coli. Microb Pathog 99:247–252. https://doi.org/10.1016/j.micpath.2016.08.033

    CAS  Article  PubMed  Google Scholar 

  4. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97(12):6640–6645. https://doi.org/10.1073/pnas.120163297

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Ding X et al (2018) The different roles of hcp1 and hcp2 of the type VI secretion system in Escherichia coli strain CE129. J Basic Microbiol 58(11):938–946. https://doi.org/10.1002/jobm.201800156

    CAS  Article  PubMed  Google Scholar 

  6. Duan Q et al (2012) The flagella of F18ab Escherichia coli is a virulence factor that contributes to infection in a IPEC-J2 cell model in vitro. Vet Microbiol 160(1–2):132–140. https://doi.org/10.1016/j.vetmic.2012.05.015

    CAS  Article  PubMed  Google Scholar 

  7. Duan Q et al (2013) Flagella from F18+ Escherichia coli play a role in adhesion to pig epithelial cell lines. Microb Pathog 55:32–38. https://doi.org/10.1016/j.micpath.2012.09.010

    CAS  Article  PubMed  Google Scholar 

  8. Dyszel JL, Soares JA, Swearingen MC, Lindsay A, Smith JN, Ahmer BM (2010) E. coli K-12 and EHEC genes regulated by SdiA. PLoS ONE. https://doi.org/10.1371/journal.pone.0008946

    Article  PubMed  PubMed Central  Google Scholar 

  9. Gao Q, Xia L, Liu J, Wang X, Gao S, Liu X (2016) DNA microarray-mediated transcriptional profiling of avian pathogenic Escherichia coli O2 strain E058 during its infection of chicken. Microb Pathog 100:1–9. https://doi.org/10.1016/j.micpath.2016.08.032

    CAS  Article  PubMed  Google Scholar 

  10. Gao Q, Xia L, Wang X, Ye Z, Liu J, Gao S (2019) SodA contributes to the virulence of avian pathogenic Escherichia coli O2 strain E058 in experimentally infected chickens. J Bacteriol 201:e006256. https://doi.org/10.1128/JB.00625-18

    Article  Google Scholar 

  11. Han X et al (2013) The luxS gene functions in the pathogenesis of avian pathogenic Escherichia coli. Microb Pathog 55:21–27. https://doi.org/10.1016/j.micpath.2012.09.008

    CAS  Article  PubMed  Google Scholar 

  12. Havens PL, Dunne WM, Burd EM (1992) Effects of human intravenous immune globulin on diarrhea caused by Shiga-like toxin I and Shiga-like toxin II in infant rabbits. Microbiol Immunol 36(10):1077–1085. https://doi.org/10.1111/j.1348-0421.1992.tb02111.x

    CAS  Article  PubMed  Google Scholar 

  13. Li J, Attila C, Wang L, Wood TK, Valdes JJ, Bentley WE (2007) Quorum sensing in Escherichia coli is signaled by AI-2/LsrR: effects on small RNA and biofilm architecture. J Bacteriol 189(16):6011–6020. https://doi.org/10.1128/JB.00014-07

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. Palaniyandi S, Mitra A, Herren CD, Zhu X, Mukhopadhyay S (2013) LuxS contributes to virulence in avian pathogenic Escherichia coli O78:K80:H9. Vet Microbiol 166(3–4):567–575. https://doi.org/10.1016/j.vetmic.2013.07.009

    CAS  Article  PubMed  Google Scholar 

  15. Reading NC, Sperandio V (2006) Quorum sensing: the many languages of bacteria. FEMS Microbiol Lett 254(1):1–11. https://doi.org/10.1111/j.1574-6968.2005.00001.x

    CAS  Article  PubMed  Google Scholar 

  16. Scaletsky IC, Silva ML, Trabulsi LR (1984) Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect Immun 45(2):534–536. https://doi.org/10.1007/BF01641732

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Smith JN et al (2008) SdiA, an N-acyl-homoserine lactone receptor, becomes active during the transit of Salmonella enterica through the gastrointestinal tract of turtles. PLoS ONE. https://doi.org/10.1371/journal.pone.0002826

    Article  PubMed  PubMed Central  Google Scholar 

  18. Smith JL, Fratamico PM, Yan X (2011) Eavesdropping by bacteria: the role of SdiA in Escherichia coli and Salmonella enterica serovar Typhimurium quorum sensing. Foodborne Pathog Dis 8(2):169–178. https://doi.org/10.1089/fpd.2010.0651

    CAS  Article  PubMed  Google Scholar 

  19. Sperandio V, Torres AG, Kaper JB (2010) Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 43(3):809–821. https://doi.org/10.1046/j.1365-2958.2002.02803.x

    Article  Google Scholar 

  20. Stecher B, Hapfelmeier S, Muller C, Kremer M, Stallmach T, Hardt WD (2004) Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun 72(7):4138–4150. https://doi.org/10.1128/IAI.72.7.4138-4150.2004

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Stecher B, Barthel M, Schlumberger MC, Haberli L, Rabsch W, Kremer M, Hardt WD (2008) Motility allows S. Typhimurium to benefit from the mucosal defence. Cell Microbiol 10(5):1166–1180. https://doi.org/10.1063/1.118856

    CAS  Article  PubMed  Google Scholar 

  22. Van Houdt R, Aertsen A, Moons P, Vanoirbeek K, Michiels CW (2006) N-acyl-l-homoserine lactone signal interception by Escherichia coli. FEMS Microbiol Lett 256(1):83–89. https://doi.org/10.1111/j.1574-6968.2006.00103.x

    CAS  Article  PubMed  Google Scholar 

  23. Walters M, Sperandio V (2006) Quorum sensing in Escherichia coli and Salmonella. Int J Med Microbiol 296(2–3):125–131. https://doi.org/10.1016/j.ijmm.2006.01.041

    CAS  Article  PubMed  Google Scholar 

  24. Wu X et al (2017) The role of the ptsI gene on AI-2 internalization and pathogenesis of avian pathogenic Escherichia coli. Microb Pathog 113:321–329. https://doi.org/10.1016/j.micpath.2017.10.048

    CAS  Article  PubMed  Google Scholar 

  25. Yang Y et al (2013) F18ab Escherichia coli flagella expression is regulated by acyl-homoserine lactone and contributes to bacterial virulence. Vet Microbiol 165(3–4):378–383. https://doi.org/10.1016/j.vetmic.2013.04.020

    CAS  Article  PubMed  Google Scholar 

  26. Yang Y et al (2014) Quorum-sensing gene luxS regulates flagella expression and Shiga-like toxin production in F18ab Escherichia coli. Can J Microbiol 60(6):355–361. https://doi.org/10.1139/cjm-2014-0178

    CAS  Article  PubMed  Google Scholar 

  27. Yang Y, Liu Y, Zhou M, Zhu G (2018a) Both quorum sensing (Qs)-I and Ii systems regulate Escherichia coli flagellin expression. Pak J Zool 50(5):1807–1813. https://doi.org/10.17582/journal.pjz/2018.50.5.1807.1813

    CAS  Article  Google Scholar 

  28. Yang Y, Zhou M, Hardwidge PR, Cui H, Zhu G (2018b) Isolation and characterization of N-acyl homoserine lactone-producing bacteria from cattle rumen and swine intestines. Front Cell Infect Microbiol. https://doi.org/10.3389/fcimb.2018.00155

    Article  PubMed  PubMed Central  Google Scholar 

  29. Yu L et al (2018) Autoinducer2 affects trimethoprim-sulfamethoxazole susceptibility in avian pathogenic Escherichia coli dependent on the folate synthesis-associate pathway. MicrobiologyOpen 7(4):e00582. https://doi.org/10.1002/mbo3.582

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Zhou M, Duan Q, Yang Y, Zhu G (2020) Use of fimbrial rod for F18ab Fimbriae+ STEC colonization to host cells. J vis Exp. https://doi.org/10.3791/61761

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by grants from the Chinese National Science Foundation Grants (Nos. 31972708, 31502075, 31873010, and 31672579), “13th Five-Year” National Key Development Program (2016YFD0501000), and the Priority Academic Program Development of Jiangsu Higher Education Institutions.

Author information

Affiliations

Authors

Contributions

ZG and YY conceived and designed the experiments. XZ, BZ, ZL, QD, and ZM performed experiments. YY and XZ wrote this paper.

Corresponding author

Correspondence to Guoqiang Zhu.

Ethics declarations

Conflict of interest

The authors and their institutions do not have any relationships that may influence or bias the results and data presented in this manuscript.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Erko Stackebrandt.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yang, Y., Zhang, X., Zhang, B. et al. Quorum sensing-1 signaling of N-hexanoyl-l-homoserine lactone contributes to virulence in avian pathogenic Escherichia coli. Arch Microbiol (2021). https://doi.org/10.1007/s00203-021-02571-5

Download citation

Keywords

  • APEC
  • AHL
  • Quorum sensing
  • Virulence