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Antagonistic effect of Lactobacillus strains against Escherichia coli and Listeria monocytogenes in milk

Published online by Cambridge University Press:  03 December 2010

Catalina Aguilar ,
Consuelo Vanegas  and
Bernadette Klotz
Catalina Aguilar
Affiliation:
Engineering Faculty, Universidad de La Sabana, Campus Puente del Común, Autopista Norte Km 7, Chía, Cundinamarca (Colombia)
Consuelo Vanegas
Affiliation:
Engineering Faculty, Universidad de La Sabana, Campus Puente del Común, Autopista Norte Km 7, Chía, Cundinamarca (Colombia)
Bernadette Klotz*
Affiliation:
Engineering Faculty, Universidad de La Sabana, Campus Puente del Común, Autopista Norte Km 7, Chía, Cundinamarca (Colombia)
*
†For correspondence; e-mail: bernadette.klotz@unisabana.edu.co
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Abstract

The current work studied four types of binary antagonist/pathogen bacterial culture system, in order to determine the effect of interaction between two strains of Lactobacillus plantarum and two food-borne pathogens, Listeria monocytogenes and Escherichia coli, in whole UHT milk at 37°C. To determine the type of interaction between the two bacterial populations in co-cultures and to evaluate the antagonistic activity of the lactic acid bacteria (LAB) on the pathogenic bacteria, the growth curves, the kinetic parameters, and the pH profiles of mono- and co-cultures were compared. The Lb. plantarum strains showed different bacteriocin-like inhibitory substance (BLIS) production, auto- and co-inducible. The antibacterial effect of neutralized supernatants of mono and co-cultures harvested at different times of incubation was assessed in order to establish the presence of bacteriocin-like inhibitory-substances (BLIS) and their possible relation to the growth inhibition of the pathogen. The LAB reduced the growth of Esch. coli and of List. monocytogenes by 4 and ∼5 log cycles, respectively and influenced other growth kinetic parameters, such as μmax and lag phase, in the different binary combinations. The growth of the LAB was not relevantly altered by simultaneous growth with the pathogenic strains showing an interaction of amensalism. The pattern of inhibition exerted by the LAB on the pathogens was different; Lb. plantarum LB279 inhibited the growth of List. monocytogenes more effectively than that of Esch. coli. The behaviour of Esch. coli in co-culture with Lb. plantarum WS4174 suggested the presence of metabolic crowding in the mechanism of growth suppression. This exploratory study showed the complexity and specific particularities of the inhibition phenomena between bacterial communities.

Keywords

Lactic acid bacteriaco-culturesinhibitionamensalismbiopreservation
Type
Research Article
Information
Journal of Dairy Research , Volume 78 , Issue 2 , May 2011 , pp. 136 - 143
Copyright
Copyright © Proprietors of Journal of Dairy Research 2010

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Footnotes

*

Present address: LEMA, Universidad de Los Andes, Carrera 1 No. 18 A 10, Bogotá, Colombia

References

Aoki, SK, Pamma, R, Hernday, A, Bickham, JE, Braaten, BA & Low, DA 2005 Contact-dependent inhibition of growth in Escherichia coli. Science 309 1245–1248CrossRefGoogle ScholarPubMed
Augustin, JC, Zuliani, V, Cornu, M & Guillier, L 2005 Growth rate and growth probability of Listeria monocytogenes in dairy, meat and seafood products in suboptimal conditions. Journal of Applied Microbiology 99 1019–1042CrossRefGoogle ScholarPubMed
Baranyi, J & Roberts, TA 1994 Review paper: A dynamic approach to predicting bacterial growth in food. International Journal of Food Microbiology 23 277–294CrossRefGoogle Scholar
Beg, QK, Vazquez, A, Ernst, J, de Menezes, MA, Bar-Joseph, Z, Barabási, AL & Oltvai, ZN 2007 Intracellular crowding defines the mode and sequence of substrate uptake by Escherichia coli and constrains its metabolic activity. Proceedings of the National Academy of Sciences 104 12663–12668CrossRefGoogle ScholarPubMed
Bredholt, S, Nesbakken, T & Holck, A 2001 Industrial application of an antilisterial strain of Lactobacillus sakei as a protective culture and its effect on the sensory acceptability of cooked, sliced, vacuum-packed meats. International Journal of Food Microbiology 66 191–196CrossRefGoogle Scholar
Breidt, F & Fleming, HP 1998 Modeling of the competitive growth of Listeria monocytogenes and Lactococcus lactis in vegetable broth. Applied and Environmental Microbiology 7 3159–3165CrossRefGoogle Scholar
Cintas, L, Casaus, P, Fernandez, F & Hernandez, PE 1998 Comparative antimicrobial activity of enterocin L50, pediocin PA-1, nisin A, and lactocin S against spoilage and foodborne pathogenic bacteria. Food Microbiology 15 289–298CrossRefGoogle Scholar
ComBase, Combined Database of Microbial Responses to Food Environments Food Standards Agency and the Institute of Food Research from the United Kingdom; the USDA Agricultural Research Service and its Eastern Regional Research Center from the United States; and the Australian Food Safety Centre of Excellence. http://www.combase.cc/ (Last accessed November 2009)Google Scholar
De Vuyst, L & Vandamme, EJ 1994 Antimicrobial potential of lactic acid bacteria. In Bacteriocins of Lactic Acid Bacteria: Microbiology, Genetics and Applications, pp. 91–142. London: Blackie Academic & ProfessionalCrossRefGoogle Scholar
Eklund, T 1989 Organic acids and esters. In Gould, G. W. (ed.), Mechanisms of action of food preservation procedures (pp. 160–200). Elsevier Science Publishers Ltd., London, UKGoogle Scholar
Faith, NG, Parniere, N, Larson, T, Lorang, TD & Luchansky, JB 1997 Viability of Escherichia coli O157:H7 in pepperoni during manufacture of sticks and the subsequent storage of slices at 21, 4 and −20°C under air, vacuum and CO2. International Journal of Food Microbiology 37 47–54CrossRefGoogle Scholar
Feresu, S & Nyati, H 1990 Fate of pathogenic and non-pathogenic Escherichia coli strains in two fermented milk products. Journal of Applied Bacteriology 69 814–821CrossRefGoogle ScholarPubMed
Fredrickson, AG 1977 Behavior of mixed cultures. Annual Review of Microbiology 31 63–87CrossRefGoogle ScholarPubMed
Fukushima, H & Gomyoda, M 1986 Inhibition of Yersinia enterocolitica serotype O3 by natural microflora of pork. Applied and Environmental Microbiology 990–994CrossRefGoogle ScholarPubMed
Gálvez, A, Abriouel, H, Lucas-López, RL & Omar, NB 2007 Bacteriocin-based strategies for food biopreservation. International Journal of Food Microbiology 120 51–70CrossRefGoogle ScholarPubMed
Jameson, JE 1962 A discussion of the dynamics of Salmonella enrichment. Journal of Hygiene 60 (2) 193–207CrossRefGoogle ScholarPubMed
Jeppesen, VF & Huss, HH 1993 Antagonistic activity of two strains of lactic acid bacteria against Listeria monocytogenes and Yersinia enterocolitica in a model fish product at 5°C. International Journal of Food Microbiology 19 179–186CrossRefGoogle Scholar
Koutsomanis, KP, Kendall, PA & Sofos, JN 2004 A comparative study on growth limits of Listeria monocytogenes as affected by temperature, pH and aw when grown in suspension or on a solid surface. Food Microbiology 21 415–422CrossRefGoogle Scholar
Leroy, F, Degeest, B & De Vuyst, L 2002 A novel area of predictive modelling : describing functionality of beneficial microorganisms in foods. International Journal of Food Microbiology 73 251–259CrossRefGoogle ScholarPubMed
Leroy, F & De Vuyst, L 1999 The presence of SALT and curing agent reduces bacteriocin production by Lactobacillus sakei CTC 494, a potential starter culture for sausage fermentation. Applied and Environmental Microbiology 5350–5356CrossRefGoogle ScholarPubMed
Malakar, PK, Martens, DE, Zwietering, MH, Beal, C & van't Riet, K 1999 Modelling the interactions between Lactobacillus curvatus and Enterobacter cloacae II. Mixed cultures and shelf life predictions. International Journal of Food Microbiology 51 67–79CrossRefGoogle ScholarPubMed
Maldonado, A, Jiménez-Díaz, R & Ruiz-Barba, J 2004 Induction of Plantaricin production in Lactobacillus plantarum NC8 after coculture with specific Gram-positive bacteria is mediated by an autoinduction mechanism. Journal of Bacteriology 1556–1564CrossRefGoogle ScholarPubMed
Martens, DE, Beal, C, Malakar, P, Zwietering, MH & van't Riet, K 1999 Modelling the interactions between Lactobacillus curvatus and Enterobacter cloacae I. Individual growth kinetics. International Journal of Food Microbiology 51 53–65CrossRefGoogle ScholarPubMed
McMullen, LM & Stiles, ME 1996 Potential use of bacteriocin-producing lactic acid bacteria in preservation of meats. Journal of Food Protection 59 (Suppl.) 64–71CrossRefGoogle ScholarPubMed
Ogunbanwo, ST, Sanni, AI & Onilude, AA 2003 Characterization of bacteriocin produced by Lactobacillus plantarum F1 and Lactobacillus brevis OG1. African Journal of Biotechnology 2 (8) 219–227Google Scholar
Ogwaro, BA, Gibson, H, Whitehead, M & Hill, DJ 2002 Survival of Escherichia coli O157:H7 in traditional African yoghurt fermentation. International Journal of Food Microbiology 79 105–112CrossRefGoogle ScholarPubMed
Pleasants, AB, Soboleva, TK, Dykes, GA, Jones, RJ & Filippov, AE 2001 Modelling of the growth of populations of Listeria monocytogenes and a bacteriocin-producing strain of Lactobacillus in pure and mixed cultures. Food Microbiology 18 605–615CrossRefGoogle Scholar
Presser, KA, Ratkowsky, DA & Ross, T 1997 Modelling the growth rate of Escherichia coli as function of pH and lactic acid concentration. Applied and Environmental Microbiology 63 (6) 2355–2360CrossRefGoogle ScholarPubMed
Quadri, LEN 2002 Regulation of antimicrobial peptide production by autoinducer mediated quorum sensing in lactic acid bacteria. Antonie Van Leeuwenhoek 82 133–145CrossRefGoogle ScholarPubMed
Rohwer, JM, Postma, PW, Kholodenko, BN & Westerhoff, HV 1998 Implications of macromolecular crowding for signal transduction and metabolite channeling. Proceedings of the National Academy of Sciences 95 10547–10552CrossRefGoogle ScholarPubMed
Rojo-Bezares, B, Sáenz, Y, Navarro, L, Zarazaga, M, Ruiz-Larrea, F & Torres, C 2007 Coculture-inducible bacteriocin activity of Lactobacillus plantarum strain J23 isolated from grape most. Food Microbiology 24 482–491CrossRefGoogle Scholar
Schiemann, DA & Olson, SA 1984 Antagonism by gram-negative bacteria to growth of Yersinia enterocolitica in mixed cultures. Applied and Enviromental Microbiology 48 539–544CrossRefGoogle ScholarPubMed
Vermeiren, L, Devlieghere, F, Vandekinderen, I & Debevere, J 2006 The interaction of the non-bacteriocinogenic Lactobacillus sakei 10A and lactocin S producing Lactobacillus sakei 148 towards Listeria monocytogenes on a model cooked ham. Food Microbiology 23 511–518CrossRefGoogle ScholarPubMed