Skip to main content
SpringerLink
Log in

Effects of Colistin and Bacteriocins Combinations on the In Vitro Growth of Escherichia coli Strains from Swine Origin

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

Abstract

Escherichia coli strains from swine origin, either susceptible or resistant to colistin, were grown under planktonic and biofilm cultures. After which, they were treated with antibacterial agents including nisin and enterocin DD14 bacteriocins, colistin and their combinations. Importantly, the combination of colistin, enterocin DD14 and nisin eradicated the planktonic and biofilm cultures of E. coli CIP54127 and the E. coli strains with colistin-resistance phenotype such as E. coli 184 (mcr-1 +) and E. coli 289 (mcr-1 −), suggesting therefore that bacteriocins from lactic acid bacteria could be used as agents with antibiotic augmentation capability.

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

Similar content being viewed by others

References

  1. Bauer-Garland J, Frye JG, Gray JT, Berrang ME, Harrison MA, Fedorka-Cray PJ (2006) Transmission of Salmonella entrica serotype Typhimurium in Poultry with or without antimicrobial selective pressure. J Appl Microbiol 100:1301–1308

    Article  Google Scholar 

  2. Gosh S, LaPara TM (2007) The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME J 1:191–203

    Article  Google Scholar 

  3. Gao L, Hu J, Zhang X, Wei L, Li S, Miao Z, Chai T (2015) Application of swine manure on agricultural fields contributes to extended-spectrum β-lactamase-producing Escherichia coli spread in Tai’an, China. Front Microbiol 14:313

    Google Scholar 

  4. Michalopoulos A, Falagas ME (2008) Colistin and polymyxin B in critical care. Crit Care Clin 24:377–391

    Article  CAS  Google Scholar 

  5. Fairbrother JM, Nadeau E, Gyles CL (2005) Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Anim Health Res Rev Conf Res Work Anim Dis 6:17–39

    Article  CAS  Google Scholar 

  6. Kempf I, Fleury MA, Drider D, Bruneau M, Sanders P, Chauvin C, Madec JY, Jouy E (2013) What do we know about resistance to colistin in Enterobacteriaceae in avian and pig production in Europe? Int J Antimicrob Agents 42:379–383

    Article  CAS  Google Scholar 

  7. Catry B, Cavaleri M, Baptiste K, Grave K, Grein K, Holm A, Jukes H, Liebana E, Navas AL, Mackay D, Magiorakos AP, Romo MA, Moulin G, Madero CM, Pomba MC, Powell M, Pyörälä S, Rantala M, Ružauskas M, Sanders P, Teale C, Threlfall EJ, Törneke K, van Duijkeren E, Edo JT (2015) Use of colistin-containing products within the European Union and European Economic Area (EU/EEA): development of resistance in animals and possible impact on human and animal health. Int J Antimicrob Agents 46:297–306

    Article  CAS  Google Scholar 

  8. Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu LF, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu JH, Shen J (2015) Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 15:424–427

    Article  Google Scholar 

  9. Changkaew K, Intarapuk A, Utrarachkij F, Nakajima C, Suthienkul O, Suzuki Y (2015) Antimicrobial resistance, extended-spectrum β-lactamase productivity, and class 1 integrons in Escherichia coli from healthy swine. J Food Prot 78:1442–1450

    Article  CAS  Google Scholar 

  10. Drider D, Rebuffat S (2011) Prokaryotic antimicrobial peptides: from genes to applications. Springer, New York

    Book  Google Scholar 

  11. Drider D, Bendali F, Naghmouchi K, Chikindas ML (2016) Bacteriocins: not only antibacterial agents. Probiotics Antimicrob Proteins. doi:10.1007/s12602-016-9223-0

    Google Scholar 

  12. Vogel L, van Oorschot E, Maas HME, Minderhoud B, Dijkshoorn L (2000) Epidemiologic typing of Escherichia coli using RAPD analysis, ribotyping and serotyping. Clin Microbiol Infect 6:82–87

    Article  CAS  Google Scholar 

  13. Liu W, Hansen N (1990) Some chemical and physical properties of nisin, a small-protein antibiotic produced by Lactococcus lactis. Appl Environ Microbiol 56:2551–2558

    CAS  Google Scholar 

  14. Al Atya AK, Drider-Hadiouche K, Ravallec R, Silvain A, Vachée A, Drider D (2015) Probiotic potential of Enterococcus faecalis strains isolated from meconium. Front Microbiol 2:227

    Google Scholar 

  15. Abriouel H, Valdivia E, Martínez-Bueno M, Maqueda M, Gálvez A (2013) A simple method for semi-preparative-scale production and recovery of enterocin AS-48 derived from Enterococcus faecalis subsp. liquefaciens A-48-32. J Microbiol Methods 55:599–605

    Article  Google Scholar 

  16. Naghmouchi K, Drider D, Kheadr E, Lacroix C, Prévost H, Fliss I (2006) Multiple characterizations of Listeria monocytogenes sensitive and insensitive variants to divergicin M35, a new pedioci-like bacteriocin. J Appl Microbiol 100:29–39

    Article  CAS  Google Scholar 

  17. CA-SFM (2013) Comité de l’antibiogramme de la société française de microbiologie. http://www.sfm-microbiologie.org/UserFiles/files/casfm/CASFM2013vjuin.pdf

  18. Aarestrup FM, Wegener HC, Collignon P (2008) Resistance in bacteria of the food chain: epidemiology and control strategies. Expert Rev Anti Infect Ther 6:733–750

    Article  Google Scholar 

  19. Suzuki S, Hoa PT (2012) Distribution of quinolones, sulfonamides, tetracyclines in aquatic environment and antibiotic resistance in Indochina. Front Microbiol 3:67

    Google Scholar 

  20. Andremont A, Fiona F (2015) What to do about resistant bacteria in the food-chain? Bull World Health Organ 93:217–218

    Article  Google Scholar 

  21. European Food Safety Authority (2012) Technical specifications on the harmonised monitoring and reporting of antimicrobial resistance in Salmonella, Campylobacter and indicator Escherichia coli and Enterococcus spp. bacteria transmitted through food. EFSA J 10:1–64

    Google Scholar 

  22. Tadesse DA, Zhao S, Tong E, Ayers S, Singh A, Bartholomew MJ, McDermott PF (2012) Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950–2002. Emerg Infect Dis 18:741–749

    Article  CAS  Google Scholar 

  23. Tadesse DA, Zhao S, Tong E, Ayers S, Singh A, Bartholomew MJ, McDermott P (2012) Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950–2002. Emerg Infect Dis 18:741–749

    Article  CAS  Google Scholar 

  24. Dijkmans AC, Wilms EB, Kamerling IM, Birkhoff W, Ortiz-Zacarías NV, van Nieuwkoop C, Verbrugh HA, Touw DJ (2015) Colistin: revival of an old polymyxin antibiotic. Ther Drug Monit 374:419–427

    Article  Google Scholar 

  25. Spapen H, Jacobs R, Van Gorp V, Troubleyn J, Honoré PM (2011) Renal and neurological side effects of colistin in critically ill patients. Ann Intensive Care 1:14

    Article  Google Scholar 

  26. Olaitan AO, Morand S, Rolain JM (2014) Mechanisms of polymyxin resistance: acquired and intrinsic resistance in bacteria. Front Microbiol 5:643

    Article  Google Scholar 

  27. Nordmann P, Jayol A, Poirel L (2016) Rapid detection of polymyxin resistance in Enterobacteriaceae. Emerg Infect Dis 22:1038–1043

    Article  Google Scholar 

  28. Arcilla MS, van Hattem JM, Matamoros S, Melles DC, Penders J, de Jong MD et al (2016) Dissemination of the mcr-1 colistin resistance gene. Lancet Infect Dis 16:147–149

    Article  Google Scholar 

  29. Guenther S, Ewers C, Wieler LH (2011) Extended-spectrum beta-lactamases producing E. coli in wildlife, yet another form of environmental pollution? Front Microbiol 2:246

    Article  Google Scholar 

  30. Breukink E, Wiedemann I, van Kraaij C, Kuipers OP, Sahl HG, de Kruijff B (1999) Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science 286:2361–2364

    Article  CAS  Google Scholar 

  31. Wiedemann I, Breukink E, vanKraaij C, Kuipers OP, Bierbaum G, deKruijff B, Sahl HG (2001) Specific binding of nisin to the peptidoglycan precursor lipid II combines pore formation and inhibition of cell wall biosynthesis for potent antibiotic activity. J Biol Chem 276:1772–1779

    Article  CAS  Google Scholar 

  32. Nissen-Meyer J, Oppegård C, Rogne P, Haugen HS, Kristiansen PE (2010) Structure and mode-of-action of the two-peptide (class-IIb) bacteriocins. Probiotics Antimicrob Proteins 1:52–60

    Article  Google Scholar 

  33. Naghmouchi N, Baah J, Hober D, Jouy E, Rubrecht C, Sané F, Drider D (2013) Synergistic effect between colistin and bacteriocins in controlling Gram-negative pathogens and their potential to reduce antibiotic toxicity in mammalian epithelial cells. Antimicrob Agents Chemother 57:2719–2725

    Article  CAS  Google Scholar 

  34. Naghmouchi N, Drider D, Baah J, Teather R (2010) Nisin A and polymyxin B as synergistic inhibitors of Gram-positive and Gram-negative bacteria. Prob Antimicrob Prot 2:98–103

    Article  CAS  Google Scholar 

  35. Naghmouchi N, Belguesmia Y, Baah J, Teather R, Drider D (2011) Antibacterial activity of class I and IIa bacteriocins combined with polymyxin E against resistant variants of Listeria monocytogenes and Escherichia coli. Res Microbiol 162:99–107

    Article  CAS  Google Scholar 

  36. Belguesmia Y, Madi A, Sperandio D, Merieau A, Feuilloley M, Prévost H, Drider D, Connil N (2011) Growing insights into the safety of bacteriocins: the case of enterocin S37. Res Microbiol 162:159–163

    Article  CAS  Google Scholar 

  37. Allen HK, Trachsel J, Looft T, Casey TA (2014) Finding alternatives to antibiotics. Ann NY Acad Sci 1323:100–191

    Article  Google Scholar 

  38. Cavera VL, Arthur TD, Kashtanov D, Chikindas ML (2015) Bacteriocins and their position in the next wave of conventional antibiotics. Int J Antimicrob Agents 46:494–501

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Ahmed Khassaf Al Atya received a PhD scholarship from the French and Iraqi governments. The authors are grateful to Campus France for providing funds and Lille 1 University for supporting visiting professorship position for Prof. Hikmate Abriouel. The authors wish to thank the RESAPATH laboratories, Dr. Sophie Granier (Anses) for the mcr-1 positive control and Dr. Benoit Cudennec for statistical analysis.

Author information

Authors and Affiliations

  1. Univ. Lille, INRA, ISA, Univ. Artois, Univ. Littoral Côte d’Opale, EA 7394 – ICV - Institut Charles Viollette, 59000, Lille, France

    Ahmed K. Al Atya & Djamel Drider

  2. Área de Microbiología, Departamento de Ciencias de la Salud, Facultad de Ciencias Experimentales, Universidad de Jaén, Jaén, Spain

    Hikmate Abriouel

  3. ANSES, Ploufragan Laboratory, Ploufragan, Univ Bretagne Loire, Rennes, France

    Isabelle Kempf & Eric Jouy

  4. Phileo Animal Care, 137 rue Gabriel Péri, 59700, Marcq-en-Barœul, France

    Eric Auclair

  5. Laboratoire de Bactériologie, Hôpital Victor Provo, Boulevard Lacordaire, 59100, Roubaix, France

    Anne Vachée

Authors
  1. Ahmed K. Al Atya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hikmate Abriouel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Isabelle Kempf
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eric Jouy
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eric Auclair
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anne Vachée
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Djamel Drider
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Djamel Drider.

Ethics declarations

Conflict of interest

Ahmed K. Al Atya, Hikmate Abriouel, Isabelle Kempf, Eric Jouy, Eric Auclair, Anne Vachée and Djamel Drider declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Al Atya, A.K., Abriouel, H., Kempf, I. et al. Effects of Colistin and Bacteriocins Combinations on the In Vitro Growth of Escherichia coli Strains from Swine Origin. Probiotics & Antimicro. Prot. 8, 183–190 (2016). https://doi.org/10.1007/s12602-016-9227-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-016-9227-9

Keywords

Search

Navigation