Skip to main content
SpringerLink
Log in

Outer Membrane Channel Protein TolC Regulates Escherichia coli K12 Sensitivity to Plantaricin BM-1 via the CpxR/CpxA Two-Component Regulatory System

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

Plantaricin BM-1, a class IIa bacteriocin produced by Lactobacillus plantarum BM-1, has significant antibacterial activity against Gram-positive and Gram-negative bacteria. This study aimed to explore the role of the Escherichia coli K12 outer membrane (OM) channel protein TolC in the response to plantaricin BM-1. The tolC null mutant (E. coli K12∆tolC) was constructed by Red homologous recombination. The mechanism of tolC regulating the sensitivity of E. coli K12 under plantaricin BM-1 was investigated. tolC null mutation significantly increased the E. coli K12 sensitivity to plantaricin BM-1 and inhibited biofilm formation, and cells ruptured and shrunk. Proteomic analysis showed that the AcrAB-TolC and EmrAB-TolC efflux pumps were significantly (p < 0.05) upregulated in E. coli K12∆tolC. Based on the results of real-time PCR, we concluded that under plantaricin BM-1, the CpxR/CpxA two-component regulatory system of E. coli K12 responded with envelope damage, followed by activation of the transcription of marA and expression of AcrAB-TolC efflux pump. Moreover, tolC null mutation weakened the AcrAB-TolC efflux pump and then increased the sensitivity of E. coli K12 to plantaricin BM-1. These will contribute exploring the action mechanism of class IIa bacteriocins against Gram-negative bacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Riley MA, Wertz JE (2002) Bacteriocins: evolution, ecology, and application. Annu Rev Microbiol 56:117–137. https://doi.org/10.1146/annurev.micro.56.012302.161024

    Article  CAS  PubMed  Google Scholar 

  2. Cleveland J, Montville TJ, Nes IF, Chikindas ML (2001) Bacteriocins: safe, natural antimicrobials for food preservation. Int J Food Microbiol 71:1–20. https://doi.org/10.1016/s0168-1605(01)00560-8

    Article  CAS  PubMed  Google Scholar 

  3. Yang SC, Lin CH, Sung CT, Fang JY (2004) Corrigendum: antibacterial activities of bacteriocins: application in foods and pharmaceuticals. Front Microbiol 5:241. https://doi.org/10.3389/fmicb.2014.00683

    Article  Google Scholar 

  4. Klaenhammer TR (1993) Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev 12:39–85. https://doi.org/10.1111/j.1574-6976.1993.tb00012.x

    Article  CAS  PubMed  Google Scholar 

  5. Drider D, Fimland G, Héchard Y, Mcmullen LM, Prévost H (2006) The continuing story of class IIa bacteriocins. Microbiol Mol Biol Rev 70:564–582. https://doi.org/10.1128/MMBR.00016-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Gravesen A, Ramnath M, Rechinger KB, Andersen N, Jansch L, Hechard Y, Hastings JW, Knøchel S (2002) High-level resistance to class IIa bacteriocins is associated with one general mechanism in Listeria monocytogenes. Microbiology 148:2361–2369. https://doi.org/10.1099/00221287-148-8-2361

    Article  CAS  PubMed  Google Scholar 

  7. Vadyvaloo V, Hastings JW, van der Merwe MJ, Rautenbach M (2002) Membranes of class IIa bacteriocin-resistant Listeria monocytogenes cells contain increased levels of desaturated and short-acyl-chain phosphatidylglycerols. Appl Environ Microbiol 68:5223–5230. https://doi.org/10.1128/AEM.68.11.5223-5230.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Nikaido H (2001) AcrAB and related multidrug efflux pumps of Escherichia coli. J Mol Microbiol Biotechnol 3:215–218. https://doi.org/10.1016/S0167-7012(00)00245-1

    Article  CAS  PubMed  Google Scholar 

  9. Kjos M, Nes IF, Diep DB (2009) Class II one-peptide bacteriocins target a phylogenetically defined subgroup of mannose phosphotransferase systems on sensitive cells. Microbiology 155:2949–2961. https://doi.org/10.1099/mic.0.030015-0

    Article  CAS  PubMed  Google Scholar 

  10. Pal G, Srivastava S (2014) Inhibitory effect of plantaricin peptides (Pln E/F and J/K) against Escherichia coli. World J Microbiol Biotechnol 30:2829–2837. https://doi.org/10.1007/s11274-014-1708-y

    Article  CAS  PubMed  Google Scholar 

  11. Vaara M (1992) Agents that increase the permeability of the outer membrane. Microbiol Rev 56:395–411. https://doi.org/10.0000/PMID1406489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Nikaido H (1996) Multidrug efflux pumps of gram-negative bacteria. J Bacteriol 178:5853–5859. https://doi.org/10.1128/jb.178.20.5853-5859.1996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Bavro VN, Pietras Z, Furnham N, Pérez-Cano L, Fernández-Recio J, Xue YP, Misra R, Luisi B (2008) Assembly and channel opening in a bacterial drug efflux machine. Mol Cell 30:114–121. https://doi.org/10.1016/j.molcel.2008.02.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Wiriyathanawudhiwong N, Ohtsu I, Li ZD, Mori H, Takagi H (2009) The outer membrane TolC is involved in cysteine tolerance and overproduction in Escherichia coli. Appl Microbiol Biotechnol 81:903–913. https://doi.org/10.1007/s00253-008-1686-9

    Article  CAS  PubMed  Google Scholar 

  15. Zhang H, Liu L, Hao Y, Zhong S, Liu H, Han T, Xie Y (2013) Isolation and partial characterization of a bacteriocin produced by Lactobacillus plantarum BM-1 isolated from a traditionally fermented Chinese meat product. Microbiol Immunol 57:746–755. https://doi.org/10.1111/1348-0421.12091

    Article  CAS  PubMed  Google Scholar 

  16. Juhas M, Ajioka JW (2016) Lambda Red recombinase-mediated integration of the high molecular weight DNA into the Escherichia coli chromosome. Microb Cell Factories 15:172. https://doi.org/10.1186/s12934-016-0571-y

    Article  CAS  Google Scholar 

  17. Cao S, Zhao F, Du R, Xiao H, Han Y, Zhou Z (2018) The mode of action of bacteriocin CHQS, a high antibacterial activity bacteriocin produced by Enterococcus faecalis TG2. Food Control 96:470–478. https://doi.org/10.1016/j.foodcont.2018.09.028

    Article  CAS  Google Scholar 

  18. Yi L, Li X, Luo L, Lu Y, Yan H, Qiao Z, Lü X (2018) A novel bacteriocin BMP11 and its antibacterial mechanism on cell envelope of Listeria monocytogenes and Cronobacter sakazakii. Food Control 91:160–169. https://doi.org/10.1016/j.foodcont.2018.03.038

    Article  CAS  Google Scholar 

  19. Wu Z, Wang G, Wang W, Pan D, Peng L, Lian L (2018) Proteomics analysis of the adhesion activity of Lactobacillus acidophilus ATCC 4356 upon growth in an intestine-like pH environment. Proteomics 18:1700308. https://doi.org/10.1002/pmic.20170030

    Article  Google Scholar 

  20. Yang W, Xie Y, Jin J, Liu H, Zhang H (2019) Development and application of an active plastic multilayer film by coating a plantaricin BM-1 for chilled meat preservation. J Food Sci 84:1864–1870. https://doi.org/10.1111/1750-3841.14608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Cotter PD, Ross RP, Hill C (2013) Bacteriocins-a viable alternative to antibiotics? Nat Rev Microbiol 11:95–105. https://doi.org/10.1038/nrmicro2937

    Article  CAS  PubMed  Google Scholar 

  22. Band VI, Weiss DS (2014) Mechanisms of antimicrobial peptide resistance in gram-negative bacteria. Antibiotics (Basel) 4:18–41. https://doi.org/10.3390/antibiotics4010018

    Article  Google Scholar 

  23. Papo N, Shai Y (2005) A molecular mechanism for lipopolysaccharide protection of gram-negative bacteria from antimicrobial peptides. J Biol Chem 280:10378–10387. https://doi.org/10.1074/jbc.m412865200

    Article  CAS  PubMed  Google Scholar 

  24. Vaara M, Nurminen M (1999) Outer membrane permeability barrier in Escherichia coli mutant that are defective in the late acyltransferases of lipid a biosynthesis. Antimicrob Agents Chemother 43:1459–1462. https://doi.org/10.1046/j.1365-2672.1998.00400.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Okuda K (2013) Effects of bacteriocins on methicillin-resistant Staphylococcus aureus biofilm. Antimicrob Agents Chemother 57:5572–5579. https://doi.org/10.1128/AAC.00888-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Gooderham WJ, Bains M, Mcphee JB, Wiegand I, Hancock REW (2008) Induction by cationic antimicrobial peptides and involvement in intrinsic polymyxin and antimicrobial peptide resistance, biofilm formation, and swarming motility of PsrA in Pseudomonas aeruginosa. J Bacteriol 190:5624–5634. https://doi.org/10.1128/JB.00594-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Zakharov SD, Wang XS, Cramer WA (2011) The colicin E1 TolC-binding conformer: pillar or pore function of TolC in colicin import? Biochemistry 55:5084–5094. https://doi.org/10.1021/acs.biochem.6b00621

    Article  CAS  Google Scholar 

  28. Weatherspoon-Griffin N, Yang D, Kong W, Hua Z, Shi Y (2014) The CpxR/CpxA two-component regulatory system up-regulates the multidrug resistance cascade to facilitate Escherichia coli resistance to a model antimicrobial peptide. J Biol Chem 289:32571–32582. https://doi.org/10.1074/jbc.M114.565762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The research was supported by the Research Project of Beijing Municipal Commission of Education (KM201810020016).

Author information

Author notes

  1. Huan Wang and Hongxing Zhang contributed equally to this work.

Authors and Affiliations

  1. Beijing Laboratory of Food Quality and Safety, Beijing Key Laboratory of Agricultural Product Detection and Control of Spoilage Organisms and Pesticide Residue, College of Food Science and Engineering, Beijing University of Agriculture, Beijing, 102206, China

    Huan Wang, Hongxing Zhang, Hanwei Zhang, Junhua Jin & Yuanhong Xie

Authors
  1. Huan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hongxing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hanwei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Junhua Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuanhong Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuanhong Xie.

Ethics declarations

Conflict of Interest

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, H., Zhang, H., Zhang, H. et al. Outer Membrane Channel Protein TolC Regulates Escherichia coli K12 Sensitivity to Plantaricin BM-1 via the CpxR/CpxA Two-Component Regulatory System. Probiotics & Antimicro. Prot. 13, 238–248 (2021). https://doi.org/10.1007/s12602-020-09671-6

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-020-09671-6

Keywords

Search

Navigation