Skip to main content

Advertisement

SpringerLink
Log in

Production of a Class IIb Bacteriocin with Broad-spectrum Antimicrobial Activity in Lactiplantibacillus plantarum RUB1

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

Abstract

Bacteriocins produced by lactic acid bacteria have potential use as natural food preservatives, which may alleviate current problems associated with the overuse of antibiotics and emerging multi-drug-resistant microbes. In this work, Lactiplantibacillus plantarum RUB1 was found to produce a class IIb bacteriocin with strong antibacterial activity. Except for plnXY encoding putative proteins, L. plantarum RUB1 contains most genes in five operons (plnABCD, plnGHSTUVW, plnMNOP, plnIEF, and plnRLJK) related to bacteriocin synthesis. Adding low (100 and 500 ng/mL) and medium (1 μg/mL) concentrations of PlnA to broth promoted bacteriocin production and upregulated bacteriocin gene plnA, while high concentrations (50 and 200 μg/mL) inhibited expression of these genes. Co-culturing L. plantarum RUB1 with Enterococcus hirae 1003, Enterococcus hirae LWS, Limosilactobacillus fermentum RC4, L. plantarum B6, and even Listeria monocytogenes ATCC 19111 and Staphylococcus aureus ATCC 6538 enhanced bacteriocin activity and expression of bacteriocin-related genes. This study verifies that PlnA can indeed upregulate the expression of bacteriocin genes, and also bacteriocin production can be induced by co-culture with some specific bacteria or their cell-free supernatants. Bacteriocin production by L. plantarum RUB1 is mediated by a quorum sensing mechanism, directly influenced by autoinducing peptide or specific strains. The findings provide new methods and insight into bacteriocin production mechanisms.

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

Similar content being viewed by others

Data Availability

All data generated or analysed during this study are included in this submitted article.

References

  1. Zendo T (2013) Screening and characterization of novel bacteriocins from lactic acid bacteria. Biosci Biotechnol Biochem 77:893–899. https://doi.org/10.1271/bbb.130014

    Article  CAS  PubMed  Google Scholar 

  2. Maeda M, Shibata A, Biswas G, Korenaga H, Kono T, Itami T, Sakai M (2014) Isolation of lactic acid bacteria from kuruma shrimp (Marsupenaeus japonicus) intestine and assessment of immunomodulatory role of a selected strain as probiotic. Mar Biotechnol (NY) 16:181–192. https://xs.scihub.ltd/https://doi.org/10.1007/s10126-013-9532-1

  3. Juturu V, Wu JC (2018) Microbial production of bacteriocins: latest research development and applications. Biotechnology Adv 8:2187–2200. https://doi.org/10.1016/j.biotechadv.2018.10.007

    Article  CAS  Google Scholar 

  4. Zimina M, Babich O, Prosekov A, Sukhikh S, Noskova S (2020) Overview of global trends in classification, methods of preparation and application of bacteriocins. Antibiotics 9:553–573. https://doi.org/10.3390/antibiotics9090553

  5. Turovskiy Y, Kashtanov D, Paskhover B, Chikindas ML (2007) Quorum sensing: fact, fiction, and everything in between. Adv Appl Microbiol 62:191–234. https://doi.org/10.1016/S0065-2164(07)62007-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Papenfort K, Bassler BL (2016) Quorum sensing signal–response systems in Gram-negative bacteria. Nat Rev Microbiol 14:576–588. https://doi.org/10.1038/nrmicro.2016.89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Abisado RG, Benomar S, Klaus JR, Dandekar AA, Chandler JR (2018) Bacterial quorum sensing and microbial community interactions. MBio 9:e02331-17. https://doi.org/10.1128/mBio.02331-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Chikindas ML, Weeks R, Drider D, Chistyakov VA, Dicks LMT (2018) Functions and emerging applications of bacteriocins. Curr Opin Biotechnol 49:23–28. https://doi.org/10.1016/j.copbio.2017.07.011

  9. Straume D, Johansen RF, Bjørås M, Nes IF, Diep DB (2009) DNA binding kinetics of two response regulators, PlnC and PlnD, from the bacteriocin regulon of Lactobacillus plantarum C11. BMC Biochem 10:17–0. https://doi.org/10.1186/1471-2091-10-17

  10. Mathiesen G, Sveen A, Brurberg MB, Fredriksen L, Axelsson L, Eijsink VG (2009) Genome-wide analysis of signal peptide functionality in Lactobacillus plantarum WCFS1. BMC Genom 10:425–438. https://doi.org/10.1186/1471-2164-10-425

    Article  CAS  Google Scholar 

  11. Navarro L, Rojo-Bezares B, Sáenz Y, Díez L, Zarazaga M, Ruiz-Larrea F, Torres C (2008) Comparative study of the pln locus of the quorum-sensing regulated bacteriocin-producing L. plantarum J51 strain. Int J Food Microbiol 128:390–394. https://doi.org/10.1016/j.ijfoodmicro.2008.08.004

    Article  CAS  PubMed  Google Scholar 

  12. Gholamzadeh M, Gharajeh NH, Hejazi MA (2019) Genetic and in silico analysis of plantaricin EFI locus in indigenous isolates of Lactobacillus plantarum. Biotechnol Prog e2773. https://doi.org/10.1002/btpr.2773

  13. Maldonado-Barragán A, Caballero-Guerrero B, Lucena-Padrós H, Ruiz-Barba JL (2013) Induction of bacteriocin production by coculture is widespread among plantaricin-producing Lactobacillus plantarum strains with different regulatory operons. Food Microbiol 33:40–47. https://doi.org/10.1016/j.fm.2012.08.009

    Article  CAS  PubMed  Google Scholar 

  14. Sturme MH, Francke C, Siezen RJ, de Vos WM, Kleerebezem M (2007) Making sense of quorum sensing in lactobacilli: a special focus on Lactobacillus plantarum WCFS1. Microbiol 153:3939–3947. https://doi.org/10.1099/mic.0.2007/012831-0

    Article  CAS  Google Scholar 

  15. Devi SM, Halami PM (2019) Genetic variation of pln loci among probiotic Lactobacillus plantarum group strains with antioxidant and cholesterol-lowering ability. Probiotics Antimicrob Proteins 11:11–22. https://doi.org/10.1007/s12602-017-9336-0

    Article  CAS  PubMed  Google Scholar 

  16. Maldonado A, Ruiz-Barba JL, Jiménez-Díaz R (2004) Production of plantaricin NC8 by Lactobacillus plantarum NC8 is induced in the presence of different types of gram-positive bacteria. Arch Microbiol 181:8–16. https://doi.org/10.1007/s00203-003-0606-8

    Article  CAS  PubMed  Google Scholar 

  17. Rojo-Bezares B, Sáenz Y, Zarazaga M, Torres C, Ruiz-Larrea F (2007) Antimicrobial activity of nisin against Oenococcus oeni and other wine bacteria. Int J Food Microbiol 116:32–36. https://doi.org/10.1016/j.ijfoodmicro.2006.12.020

    Article  CAS  PubMed  Google Scholar 

  18. Maldonado-Barragan A, Caballero-Guerrero B, Lucena-Padros H, Ruiz-Barba JL (2013) Induction of bacteriocin production by coculture is widespread among plantaricin-producing Lactobacillus plantarum strains with different regulatory operons. Food Microbiol 33:40–47. https://doi.org/10.1016/j.fm.2012.08.009

    Article  CAS  PubMed  Google Scholar 

  19. Liu JJ, Wang YP, Li AY, Iqbal M, Zhang LH, Pan HC, Liu ZG, Li JK (2020) Probiotic potential and safety assessment of Lactobacillus isolated from yaks. Microb Pathog 145:104213. https://doi.org/10.1016/j.micpath.2020.104213

    Article  CAS  PubMed  Google Scholar 

  20. Diep DB, Håvarstein LS, Nes IF (1995) A bacteriocin-like peptide induces bacteriocin synthesis in Lactobacillus plantarum C11. Mol Microbiol 18:631–639. https://doi.org/10.1111/j.1365-2958.1995.mmi_18040631.x

    Article  CAS  PubMed  Google Scholar 

  21. Wang CY, Xu GD, Wen Q, Peng XL, Chen OG, Zhang JW et al (2019) CBS promoter hypermethylation increases the risk of hypertension and stroke. Clinics 74:e630. https://doi.org/10.6061/clinics/2019/e630

    Article  PubMed  PubMed Central  Google Scholar 

  22. Diep DB, Straume D, Kjos M, Torres C, Nes IF (2009) An overview of the mosaic bacteriocin pln loci from Lactobacillus plantarum. Peptides 30:1562–1574. https://doi.org/10.1016/j.peptides.2009.05.014

    Article  CAS  PubMed  Google Scholar 

  23. Sáenz Y, Rojo-Bezares B, Navarro L, Díez L, Somalo S, Zarazaga, M, Ruiz-Larrea F, Torres C (2009) Genetic diversity of the pln locus among oenological Lactobacillus plantarum strains. Int J Food Microbiol 134:76–183. https://doi.org/10.1016/j.ijfoodmicro.2009.06.004

  24. Todorov SD, Dicks LMT (2006) Screening for bacteriocin-producing lactic acid bacteria from boza, a traditional cereal beverage from Bulgaria: comparison of the bacteriocins. Process Biochem (Oxford, U. K.) 41:11–19. https://doi.org/10.1016/j.procbio.2005.01.026

  25. Wieckowicz M, Schmidt M, Sip A, Grajek W (2011) Development of a PCR-based assay for rapid detection of class IIa bacteriocin genes. Lett Appl Microbiol 52:281–289. https://doi.org/10.1111/j.1472-765X.2010.02999.x

    Article  CAS  PubMed  Google Scholar 

  26. Yi HX, Zhang LW, Tuo YF, Han X, Du M (2010) A novel method for rapid detection of class IIa bacteriocin-producing lactic acid bacteria. Food Control 21:426–430. https://doi.org/10.1016/j.foodcont.2009.07.002

  27. Zouhir A, Hammami R, Fliss I, Ben Hamida J (2010) A new structure-based classification of Gram-positive bacteriocins. Protein J 29:432–439. https://doi.org/10.1007/s10930-010-9270-4

    Article  CAS  PubMed  Google Scholar 

  28. Alvarez-Sieiro P, Montalbán-López M, Mu DD, Kuipers OP (2016) Bacteriocins of lactic acid bacteria: extending the family. Appl Microbiol Biotechnol 100:2939–2951. https://doi.org/10.1007/s00253-016-7343-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ruiz-Barba JL, Caballero-Guerrero B, Maldonado-Barragán A, Jiménez-Díaz R (2010) Coculture with specific bacteria enhances survival of Lactobacillus plantarum NC8, an autoinducer-regulated bacteriocin producer, in olive fermentations. Food Microbiol 27:413–417. https://doi.org/10.1016/j.fm.2009.10.002

    Article  CAS  PubMed  Google Scholar 

  30. Anderssen EL, Diep DB, Nes IF, Eijsink VGH, Nissen-Meyer J (1998) Antagonistic activity of Lactobacillus plantarum C11: two new two-peptide bacteriocins, plantaricins EF and JK, and the induction factor plantaricin A. Appl Environ Microbiol 64:2269–2272. http://aem.asm.org/https://doi.org/10.1128/aem.64.6.2269-2272.1998

  31. Hauge HH, Mantzilas D, Moll GN, Konings WN, Driessen AJM, Eijsink VGH, Nissen-Meyer J (1998) Plantaricin A is an amphiphilic α-helical bacteriocin-like pheromone which exerts antimicrobial and pheromone activities through different mechanisms. Biochemistry 37:16026–16032. https://doi.org/10.1021/bi981532j

    Article  CAS  PubMed  Google Scholar 

  32. Nilsen T, Nes IF, Holo H (1998) An exported inducer peptide regulates bacteriocin production in Enterococcus faecium CTC492. J Bacteriol 180:1848–1854. https://doi.org/10.1128/JB.180.7.1848-1854.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Domínguez-Manzano J, Jiménez-Díaz R (2013) Suppression of bacteriocin production in mixed-species cultures of lactic acid bacteria. Food control 30:474–479. https://doi.org/10.1016/j.foodcont.2012.09.014

    Article  CAS  Google Scholar 

  34. Maldonado A, Jiménez-Díaz R, Ruiz-Barba JL (2004) Induction of plantaricin production in Lactobacillus plantarum NC8 after coculture with specific Gram-positive bacteria is mediated by an autoinduction mechanism. J Bacteriol 186:1556–1564. https://doi.org/10.1128/JB.186.5.1556-1564.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Jain PK, McNaught CE, Anderson ADG, MacFie J, Mitchell CJ (2004) Influence of synbiotic containing Lactobacillus acidophilus La5, Bifidobacterium lactis Bb 12, Streptococcus thermophilus, Lactobacillus bulgaricus and oligofructose on gut barrier function and sepsis in critically ill patients: a randomised controlled trial. Clin Nutr 23:467–475. https://doi.org/10.1016/j.clnu.2003.12.002

    Article  PubMed  Google Scholar 

  36. Xue T, Zhao LP, Sun BL (2013) LuxS/AI-2 system is involved in antibiotic susceptibility and autolysis in Staphylococcus aureus NCTC 8325. Int J Antimicrob Agents 41:85–89. https://doi.org/10.1016/j.ijantimicag.2012.08.016

    Article  CAS  PubMed  Google Scholar 

  37. Siller M, Janapatla RP, Pirzada ZA, Hassler C, Zinkl D, Charpentier E (2008) Functional analysis of the group a streptococcal luxS/AI-2 system in metabolism, adaptation to stress and interaction with host cells. BMC Microbiol 8:188–205. https://doi.org/10.1186/1471-2180-8-188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This study received financial support from the National Natural Science Foundation of China (32072195, 31972048, 41406165, 41641052), the Science and Technology Department of Zhejiang Province (LGN19C200011, 2019C02085), and the Bureau of Science and Technology of Ningbo City (202002N3068).

Author information

Authors and Affiliations

  1. State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo, 315211, China

    Aijuan Wu, Yaqian Fu, Lingyu Kong, Qiyuan Shen, Mingxue Liu, Xiaoqun Zeng, Zhen Wu, Yuxing Guo & Daodong Pan

  2. Key Laboratory of Animal Protein Food Processing Technology of Zhejiang Province, College of Food and Pharmaceutical Sciences, Ningbo University, Ningbo, 315800, China

    Aijuan Wu, Yaqian Fu, Lingyu Kong, Qiyuan Shen, Mingxue Liu, Xiaoqun Zeng, Zhen Wu & Daodong Pan

  3. Food Science and Nutrition Department, Nanjing Normal University, Nanjing, 210097, China

    Yuxing Guo

Authors
  1. Aijuan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yaqian Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lingyu Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qiyuan Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mingxue Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaoqun Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhen Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yuxing Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Daodong Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A. W., X. Z., and D. P. designed the experiments. A. W., Y. F., X. Z., and M. L. performed the experiments. A. W., L. K., Q. S., Z. W., and Y. G. performed data analysis. A. W., X. Z., and M. L. wrote the manuscript.

Corresponding author

Correspondence to Xiaoqun Zeng.

Ethics declarations

Ethical Approval

This work does not contain any studies related to human participants or animals.

Conflict of Interest

The authors declare 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

Wu, A., Fu, Y., Kong, L. et al. Production of a Class IIb Bacteriocin with Broad-spectrum Antimicrobial Activity in Lactiplantibacillus plantarum RUB1. Probiotics & Antimicro. Prot. 13, 1820–1832 (2021). https://doi.org/10.1007/s12602-021-09815-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-021-09815-2

Keywords

Search

Navigation