Food Science and Biotechnology

, Volume 21, Issue 3, pp 775–784 | Cite as

Inhibitory effects of antagonistic compounds produced from Lactobacillus brevis MLK27 on adhesion of Listeria monocytogenes KCTC3569 to HT-29 cells

Research Article

Abstract

Among lactic acid bacteria (LAB) isolated from mustard leaf kimchi, MLK27 was the most efficient strain in terms of adhesion to HT-29 cells. Competitive, exclusive, and displaceable inhibition of Listeria monocytogenes KCTC 3569 adhesion by LAB was strain-dependent. MLK27 strain displayed the highest adhesion inhibition against L. monocytogenes and produced organic acids, hydrogen peroxide, and bacteriocin. Cell-free culture supernatants (100 μL/mL) and bacteriocin (1,280 AU/mL) of MLK27 strain strongly inhibited viable cell counts of L. monocytogenes adhered to HT-29 cells. However, there was no inhibitory effect of pathogen adhesion by bacteriocin treated with protease and inhibition activity of pathogen adhesion was partially decreased by heat-treated bacteriocin. According to biochemical and phylogenetic analysis, MLK27 strain was identified as Lactobacillus brevis MLK27. In conclusion, our results have shown that L. brevis MLK27 has ability to establish in human gastrointestinal tract and to prevent pathogenic L. monocytogenes infections, which is able to be considered as probiotic strains.

Keywords

adhesion bacteriocin hydrogen peroxide Lactobacillus brevis Listeria monocytogenes 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Shah NP. Functional cultures and health benefits. Int. Dairy J. 17: 1262–1277 (2007)CrossRefGoogle Scholar
  2. 2.
    Servin AL. Adhesion of probiotic strains to the intestinal mucosa and interaction with pathogens. Best Pract. Res. Cl. Ga. 17: 741–754 (2003)CrossRefGoogle Scholar
  3. 3.
    Granato D, Perotti F, Masserey I. Cell surface-associated lipoteichoic acid acts as an adhesion factor for attachment of Lactobacillus johnsonii La1 to human enterocyte-like Caco-2 cells. Appl. Environ. Microb. 65: 1071–1077 (1999)Google Scholar
  4. 4.
    Del Re B, Sgorbati B, Miglioli M, Palenzona, D. Adhesion, autoaggregation, and hydrophobicity of 13 strains of Bifidobacterium longum. Lett. Appl. Microbiol. 31: 438–442 (2000)CrossRefGoogle Scholar
  5. 5.
    Chen X, Xu J, Shuai J, Chen J, Zhang Z, Fang W. The S-layer proteins of Lactobacillus crispatus strain ZJ001 is responsible for competitive exclusion against Escherichia coli O157:H7 and Salmonella Typhimurium. Int. J. Food Microbiol. 115: 307–312 (2007)CrossRefGoogle Scholar
  6. 6.
    Johnson-Henry KC, Hagen KE, Gordonpour M, Tompkins TA, Sherman PM. Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cell Microbiol. 9: 356–367 (2007)CrossRefGoogle Scholar
  7. 7.
    Ouwehand AC, Kirjavainen PV, Gronlund MM, Isolauri E, Salminen SJ. Adhesion of probiotic microorganisms to intestinal mucus. Int. Dairy J. 9: 623–630 (1999)CrossRefGoogle Scholar
  8. 8.
    Coconnier MH, Bernet MF, Chauviere G, Servin AL. Adhering heat-killed human Lactobacillus acidophilus, strain LB, inhibits the process of pathogenicity of diarrhoeagenic bacteria in cultures human intestinal cells. J. Diarrhoeal Dis. Res. 11: 235–242 (1993)Google Scholar
  9. 9.
    Ouwenhand AC, Isolauri E, Kirjavainen PV, Tolkko S, Salminen SJ. The mucus binding of Bifidobacterium lactis Bb12 is enhanced in the presence of Lactobacillus GG and Lactobacillus delbrueckii subsp. bulgaricus. Lett. Appl. Microbiol. 30: 10–13 (2000)CrossRefGoogle Scholar
  10. 10.
    Bernet MF, Brassart D, Neeser JR, Servin AL. Adhesion of human bifidobacterial strains to cultured human intestinal epithelial cells and inhibition of enteropathogen-cell interactions. Appl. Environ. Microb. 59: 4121–4128 (1993)Google Scholar
  11. 11.
    Gueimonde M, Jalonen L, He F, Hiramatsu M, Salminen S. Adhesion and competitive inhibition and displacement of human enteropathogens by selected lactobacilli. Food Res. Int. 39: 467–471 (2006)CrossRefGoogle Scholar
  12. 12.
    Collado MC, Meriluoto J, Salminen S. Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus. Lett. Appl. Microbiol. 45: 454–460 (2007)CrossRefGoogle Scholar
  13. 13.
    Lin CK, Tsai HC, Lin PP, Tsen HY, Tsai CC. Lacobacillus acidophilus LAP5 able to inhibit the Salmonella choleraesuis invasion to the human Caco-2 epithelial cell. Anaerobe 14: 251–255 (2008)CrossRefGoogle Scholar
  14. 14.
    Reid G, Howard J, Gan BS. Can bacterial interference prevent infection? Trends Microbiol. 9: 424–428 (2001)CrossRefGoogle Scholar
  15. 15.
    Caplice E, Fitzgerald GF. Food fermentation: Role of microorganisms in food production and preservation. Int. J. Food Microbiol. 50: 131–149 (1999)CrossRefGoogle Scholar
  16. 16.
    Mundt JO. Bergey’s manual of systematic bacteriology. pp. 577–592. In: Lactobacillus. Sneath PHA, Mair NS, Sharpe ME, Holt JG (eds). Williams & Wilkins, Baltimore, MD, USA ( 1986)Google Scholar
  17. 17.
    Elliot SN, Buret A, McKnight W, Miller MJS, Wallace JL. Bacteria rapidly colonize and modulate healing of gastric ulcers in rats. Am. J. Physiol. 275: G425–G432 (1998)Google Scholar
  18. 18.
    Tuomola EM, Salminen SJ. Adhesion of some probiotic and dairy Lactobacillus strains to Caco-2 cell cultures. Int. J. Food Microbiol. 41: 45–51 (1998)CrossRefGoogle Scholar
  19. 19.
    Frece J, Kos B, Svetec IK, Zgaga Z, Mrsa V, Suskovic J. Importance of S-layer proteins in probiotic activity of Lactobacillus acidophilus M92. J. Appl. Microbiol. 98: 285–292 (2005)CrossRefGoogle Scholar
  20. 20.
    Lee YK, Puong KY. Competition for adhesion between probiotics and human gastrointestinal pathogens in the presence of carbohydrate. Brit. J. Nutr. 88: S101–S108 (2002)CrossRefGoogle Scholar
  21. 21.
    Sherman PM, Johnson-Henry KC, Yeung HP, Ngo PSC, Goulet J, Tompkins TA. Probiotics reduce enterohemorrhagic Escherichia coli O157:H7- and enteropathogenic E. coli O126:H6-induced changes in polarized T84 epithelial cell monolayers by reducing bacterial adhesion and cytoskeletal rearrangements. Infect. Immun. 73: 5183–5188 (2005)CrossRefGoogle Scholar
  22. 22.
    Coconnier MH, Bernet MF, Kerneis S, Chauviere G, Fourniat J, Servin AL. Inhibition of adhesion of enteroinvasive pathogens to human intestinal Caco-2 cells by Lactobacillus acidophilus strain LB decreases bacterial invasion. FEMS Microbiol. Lett. 110: 299–305 (1993)CrossRefGoogle Scholar
  23. 23.
    De Vuyst L, Vandamme EJ. Influence of the carbon source on nisin production in Lactococcus lactis subsp. lactis batch fermentations. J. Gen. Microbiol. 138: 571–578 (1992)Google Scholar
  24. 24.
    Podolak PK, Zayas JF, Kastner CL, Fung DYC. Inhibition of Listeria monocytogenes and Escherichia coli O157:H7 on beef by application of organic acids. J. Food Protect. 59: 370–373 (1996)Google Scholar
  25. 25.
    Ammor S, Tauveron G, Dufour E, Chevallier I. Antibacterial activity of lactic acid bacteria against spoilage and pathogenic bacteria isolated from the same meat small-scale facility. 1-Screening and characterization of the antibacterial compounds. Food Control 17: 454–461 (2006)CrossRefGoogle Scholar
  26. 26.
    Kong S, Davison AJ. The role of interactions between O2, H2, OH, e, and O2− in free radical damage to biological systems. Arch. Biochem. Biophys. 204: 18–29 (1980)CrossRefGoogle Scholar
  27. 27.
    Sanders ME, Klaenhammer TR. The scientific basis of Lactobacillus acidophilus NCFM functionality as a probiotic. J. Dairy Sci. 84: 319–331 (2001)CrossRefGoogle Scholar
  28. 28.
    Montville TJ, Winkowski K, Ludescher RD. Models and mechanisms for bacteriocin action and application. Int. Dairy. J. 5: 797–814 (1995)CrossRefGoogle Scholar
  29. 29.
    Davidson PM, Hoover DG. Lactic acid bacteria. pp. 127–159. In: Antimcrobial Components from Lactic Acid Bacteria. Salminen S, von Wright A (eds). Marcel Dekker, New York, NY, USA (1993)Google Scholar
  30. 30.
    Kang TK, Kim WJ. Characterization of an amylase-sensitive bacteriocin DF01 produced by Lactobacillus brevis DF01 isolated from dongchimi, Korean fermented vegetable. Korean J. Food Sci. An. 30: 795–803 (2010)Google Scholar
  31. 31.
    Uymaz B, Akkoc N, Akcelik M. Partial characterization of bacteriocins produced by two Lactobacillus strains with probiotic properties. Acta Biol. Hung. 62: 95–105 (2011)CrossRefGoogle Scholar
  32. 32.
    Coventry MJ, Wan J, Gordon JB, Mawson RF, Hickey MW. Production of brevicin 286 by Lactobacillus brevis VB286 and partial characterization. J. Appl. Bacteriol. 80: 91–98 (1996)CrossRefGoogle Scholar
  33. 33.
    Benoit V, Lebrihi A, Milliere JB, Lefebvre G. Purification and partial amino acid sequence of brevicin 27, a bacteriocin produced by Lactobacillus brevis SB27. Curr. Microbiol. 34: 173–179 (1997)CrossRefGoogle Scholar
  34. 34.
    Gopal PK, Prasad J, Smart J, Gill HS. In vitro adherence properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 strains and their antagonistic activity against an enterotoxigenic Escherichia coli. Int. J. Food Microbiol. 67: 207–216 (2001)CrossRefGoogle Scholar
  35. 35.
    Lehto EM, Salminen SJ. Inhibition of Salmonella Typhimurium adhesion to Caco-2 cell cultures by Lactobacillus strains G spent culture supernate: Only a pH effect? FEMS Immunol. Med. Mic. 18: 125–132 (1997)CrossRefGoogle Scholar
  36. 36.
    Trejo FM, Minnaard J, Perez PF, De Antoni GL. Inhibition of Clostridium difficile growth and adhesion to enterocytes by Bifidobacterium supernatants. Anaerobe 12: 186–193 (2006)CrossRefGoogle Scholar
  37. 37.
    Collins MD, Gibson GR. Probiotics, prebiotics, and symbiotics: Approaches for modulating the microbial ecology of the gut. Am. J. Clin. Nutr. 69: 1052S–1057S (1999)Google Scholar

Copyright information

© The Korean Society of Food Science and Technology and Springer Netherlands 2012

Authors and Affiliations

  1. 1.Department of Food Science & TechnologyTongmyong UniversityBusanKorea
  2. 2.College of Pharmacy and Resarch Institute for Drug DevelopmentPusan National UniversityBusanKorea

Personalised recommendations