Antimicrobial Activity Of Bifidobacterial Cells And Supernatant Against B. Cereus ATCC 9884
Keywords:
Bifidobacteria, Bacillus cereus, Antagonistic capacity, Concentrated supernatant, Organic solvents, Bacteriocin-like activity
Abstract
The aim of this work was to test three experimental strains (isolated from the faeces of exclusively breast-fed babies: Bbv1, Bbv2 and BLE) and a reference strain (BLR) of bifidobacteria for their antagonistic capacity towards Bacillus cereus ATCC 9884. The antagonism of these strains was studied using two methods: one consisted of co-cultivating them at 37°C with B. cereus and the other of bringing the concentrated supernatant of their culture into contact with that of B. cereus at 37 and 6°C. The effect of a series of organic solvents on the inhibitory power of bifidobacteria strains towards B. cereus was also explored. The results obtained indicate that at 37°C, the concentrated supernatants from bifidobacteria cultures exert an antagonistic effect towards B. cereus that is much greater than that observed when bifidobacteria strains are co-cultured with the pathogen strain under study. At low temperatures (6°C), the inhibitory power of the concentrated supernatants of the bifidobacteria cultures on B. cereus is greatly reduced and spread out over time, since 48h of contact allows only 60% inhibition on average. The speed of inhibition of B. cereus by bifidobacteria supernatants also highlights this latency of action at 6°C. Organic solvents such as formaldehyde, chloroform, acetone, hexane, isobutanol, methanol and diethyl ether had no effect on the antagonism of the concentrated supernatants from the bifidobacteria cultures tested against this pathogenic germ. This suggests that these solvents do not denature protein substances with antagonistic (i.e. bacteriocin-like) activity.
References
1. Abriouel, H., Maqueda, M., Gálvez, A., Martínez-Bueno, M. and Valdivia, E. (2002): Inhibition of Bacterial Growth, Enterotoxin Production, and Spore Outgrowth in Strains of Bacillus cereus by Bacteriocin AS-48. Appl. Environ. Microbiol. 68(3): 1473–1477.
2. BENGHARBI, Z., DAHMOUNI, S., BENABDELMOUMENE, D., BENAMAR, N., FODIL, K., & SOLTANI, F. AIn Vitro Assessment Of Aloe Vera Leaf Extracts As Natural Alternatives To Antibiotics Against Pathogenic Bacteria E. Coli, S. Aureus, and P. Aeruginosa.
3. Bielecka, M., Biedrezyck, E., Sloragiewic, Z. and Smieszek M. (1998): Interaction of Bifidobacterium and Salmonella during associated growth. Int. J. Food. Microbiol. 45: 151-155.
4. De Kwaadsteniet, M. Todorov, S.D. Knoetze, H. and Dicks, L.M.T. (2005): Characterization of a 3944 Da bacteriocin, produced by Enterococcus mundtii ST15, with activity against Gram-positive and Gram-negative bacteria. Int. J. Food Microbiol. 105: 433– 444.
5. Delcenserie, V., Gavini, F., Beerens, H., Tresse, O., Franssen, C. and Daube, G. (2007): Description of a new species, Bifidobacterium crudilactis sp. nov., isolated from raw milk and raw milk cheeses. Syst. Appl. Microbiol. (Article in press).
6. Drobniewski, F.A. (1993): Bacillus cereus and related species, Clin. Microbiol. Rev. 6: 324–338.
7. Enan, G. (2000) : Inhibition of Bacillus cereus ATCC 14579 by plantaricin UG1 in vitro and in food. Nahrung. 44 (5): S. 364 – 367.
8. Fooks, L. J. and Gibson, G. R. (2003): Mixed culture fermentation studies on the effects of synbiotics on the human intestinal pathogens Campylobacter jejuni and Escherichia coli. Anaerobe. 9: 231–242.
9. Gagnon, M., Kheadr, E. E., Le Blay, G., and Fliss, I. (2004): In vitro inhibition of Escherichia coli O157:H7 by bifidobacterial strains of human origin. Int. J. Food Microbiol. 92: 69–78.
10. Garcia, M.T., Ben Omar, N., Lucas, R., Pierez-Pulido, R., Castro, A., Grande, M.J., Martinez-Canamero, M. and Galvez A. (2003): Antimicrobial activity of enterocin EJ97 on Bacillus coagulans CECT 12. Food Microbiol. 20 : 533–536
11. Garro, M. S., Aguirre, L. and De Giori, G. S. (2006): Biological activity of Bifidobacterium longum in response to environmental pH. Appl. Microbiol. Biotechnol. 70: 612–617.
12. Grande, M. J., Lucas, R., Abriouel, H., Valdivia, E., Ben Omar, N., Maqueda, M., Martinez-Bueno, M., Martinez-Canamero, M. and Galvez, A. (2006): Inhibition of toxicogenic Bacillus cereus in rice-based foods by enterocin AS-48. Int. J. Food Microbiol. 106: 185 – 194.
13. Granum, P.E. (1997): Bacillus cereus, in: Fundamentals in Food Microbiology, ASM, Washington, DC, pp. 327–336.
14. Granum, P.E. and Lund, T. (1997): Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Let. 157: 223–228.
15. Holzapfel, W.H., Geisen, R. and Schillinger U. (1995): Biological preservation of foods with reference to protective cultures, bacteriocins and food-grade enzymes. Food Microbiol. 24 : 343-362.
16. Ibrahim, S. and Bezkorovainy, A. (1993): Inhibition of Escherichia coli by bifidobacteria. J. Food Prot. 56: 713–715.
17. Kanbe, M. (1991): Use of intestinal lactic acid bacteria and health. In: Nakazawa, Y., Hosono, A. (Eds.), Function of Fermented Milk. Elsevier, London, United Kingdom, pp. 103– 126. Chapter 13.
18. Klaenhammer, T. R. (1988): Bacteriocins of lactic acid bacteria. Biochimie 70 : 337-349.
19. Kramer, J. M. and Gilbert, R. J. (1989): Bacillus cereus and other Bacillus species. In: Doyle, M.P. (Ed.), Foodborne Bacterial Pathogens. Marcel Dekker, New York, pp. 21–70.
20. Makras, L. and De Vuyst, L. (2006): The in vitro inhibition of Gram-negative pathogenic bacteria by bifidobacteria is caused by the production of organic acids. Int. Dairy J. 16: 1049–1057.
21. Mc Naught, C.E. and Macfie, J. (2001): Probiotics in clinical practice: a critical review of the evidence. Nutr. Res. 21: 343– 353.
22. Messi, P., Bondi, M., Sabia, C., Battini, R. and Manicardi, G. (2001): Detection and preliminary characterization of a bacteriocin (plantaricin 35d) produced by a Lactobacillus plantarum strain. Int. J. Food Microbiol. 64: 193–198.
23. Millette, M., Le Tien, C., Smoragiewicz, W. and Lacroix, M. (2007): Inhibition of Staphylococcus aureus on beef by nisin-containing modiWed alginate Wlms and beads. Food Control 18: 878–884.
24. Naimushin, A. N., Soelberg, S. D., Nguyen, D. K., Dunlap, L., Bartholomew, D., Elkind, J., Melendez, J.and Furlong, C. E. (2002): Detection of Staphylococcus aureus enterotoxin B at femtomolar levels with a miniature integrated two-channel surface plasmon resonance (SPR) sensor. Biosensors and Bioelectronics 17: 573-/584.
25. Noriega, L., Gueimonde, M., Alonso, L. and De Los Reyes-Gavilan C. G. (2003): Inhibition of Bacillus cereus growth in carbonated fermented bifidus milk. Food Microbiol. 20: 519–526.
26. Orrhage, K. and Nord, C.E. (2000): Bifidobacteria and lactobacilli in human health. Drugs Exp. Clin. Res. 26: 95–111.
27. Rosenquist, H., Smidt, L., Andersen, S. R., Jensen, G. B. and Wilcks, A. (2005): Occurrence and significance of Bacillus cereus and Bacillus thuringiensis in ready-to-eat food. FEMS Microbiol. Let. 250: 129–136
28. Rossland, E., Borge, G. I. A., Langsrud, T. and Sorhaug T. (2003): Inhibition of Bacillus cereus by strains of Lactobacillus and Lactococcus in milk. Int. J. Food Microbiol. 89: 205– 212.
29. Rossland, E., Langsrud, T., Granum, P. E. and Sbrhaug, T. (2005): Production of antimicrobial metabolites by strains of Lactobacillus or Lactococcus co-cultured with Bacillus cereus in milk. Int. J. Food Microbiol. 98: 193– 200.
30. Servin, A. (2004): Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev. 28: 405–440.
31. Svensson, B., Monthan, A., Shaheen, R., Andersson, M. A., Salkinoja-Salonen, M. and Christiansson, A. (2006): Occurrence of emetic toxin producing Bacillus cereus in the dairy production chain. Int. Dairy J. 16: 740–749.
32. Topisirovic, L., Kojic, M., Fira, D., Golic, N., Strahinic, I. and Lozo, J. (2006): Potential of lactic acid bacteria isolated from specific natural niches in food production and preservation. Int. J. Food Microbiol. 112: 230–235.
2. BENGHARBI, Z., DAHMOUNI, S., BENABDELMOUMENE, D., BENAMAR, N., FODIL, K., & SOLTANI, F. AIn Vitro Assessment Of Aloe Vera Leaf Extracts As Natural Alternatives To Antibiotics Against Pathogenic Bacteria E. Coli, S. Aureus, and P. Aeruginosa.
3. Bielecka, M., Biedrezyck, E., Sloragiewic, Z. and Smieszek M. (1998): Interaction of Bifidobacterium and Salmonella during associated growth. Int. J. Food. Microbiol. 45: 151-155.
4. De Kwaadsteniet, M. Todorov, S.D. Knoetze, H. and Dicks, L.M.T. (2005): Characterization of a 3944 Da bacteriocin, produced by Enterococcus mundtii ST15, with activity against Gram-positive and Gram-negative bacteria. Int. J. Food Microbiol. 105: 433– 444.
5. Delcenserie, V., Gavini, F., Beerens, H., Tresse, O., Franssen, C. and Daube, G. (2007): Description of a new species, Bifidobacterium crudilactis sp. nov., isolated from raw milk and raw milk cheeses. Syst. Appl. Microbiol. (Article in press).
6. Drobniewski, F.A. (1993): Bacillus cereus and related species, Clin. Microbiol. Rev. 6: 324–338.
7. Enan, G. (2000) : Inhibition of Bacillus cereus ATCC 14579 by plantaricin UG1 in vitro and in food. Nahrung. 44 (5): S. 364 – 367.
8. Fooks, L. J. and Gibson, G. R. (2003): Mixed culture fermentation studies on the effects of synbiotics on the human intestinal pathogens Campylobacter jejuni and Escherichia coli. Anaerobe. 9: 231–242.
9. Gagnon, M., Kheadr, E. E., Le Blay, G., and Fliss, I. (2004): In vitro inhibition of Escherichia coli O157:H7 by bifidobacterial strains of human origin. Int. J. Food Microbiol. 92: 69–78.
10. Garcia, M.T., Ben Omar, N., Lucas, R., Pierez-Pulido, R., Castro, A., Grande, M.J., Martinez-Canamero, M. and Galvez A. (2003): Antimicrobial activity of enterocin EJ97 on Bacillus coagulans CECT 12. Food Microbiol. 20 : 533–536
11. Garro, M. S., Aguirre, L. and De Giori, G. S. (2006): Biological activity of Bifidobacterium longum in response to environmental pH. Appl. Microbiol. Biotechnol. 70: 612–617.
12. Grande, M. J., Lucas, R., Abriouel, H., Valdivia, E., Ben Omar, N., Maqueda, M., Martinez-Bueno, M., Martinez-Canamero, M. and Galvez, A. (2006): Inhibition of toxicogenic Bacillus cereus in rice-based foods by enterocin AS-48. Int. J. Food Microbiol. 106: 185 – 194.
13. Granum, P.E. (1997): Bacillus cereus, in: Fundamentals in Food Microbiology, ASM, Washington, DC, pp. 327–336.
14. Granum, P.E. and Lund, T. (1997): Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Let. 157: 223–228.
15. Holzapfel, W.H., Geisen, R. and Schillinger U. (1995): Biological preservation of foods with reference to protective cultures, bacteriocins and food-grade enzymes. Food Microbiol. 24 : 343-362.
16. Ibrahim, S. and Bezkorovainy, A. (1993): Inhibition of Escherichia coli by bifidobacteria. J. Food Prot. 56: 713–715.
17. Kanbe, M. (1991): Use of intestinal lactic acid bacteria and health. In: Nakazawa, Y., Hosono, A. (Eds.), Function of Fermented Milk. Elsevier, London, United Kingdom, pp. 103– 126. Chapter 13.
18. Klaenhammer, T. R. (1988): Bacteriocins of lactic acid bacteria. Biochimie 70 : 337-349.
19. Kramer, J. M. and Gilbert, R. J. (1989): Bacillus cereus and other Bacillus species. In: Doyle, M.P. (Ed.), Foodborne Bacterial Pathogens. Marcel Dekker, New York, pp. 21–70.
20. Makras, L. and De Vuyst, L. (2006): The in vitro inhibition of Gram-negative pathogenic bacteria by bifidobacteria is caused by the production of organic acids. Int. Dairy J. 16: 1049–1057.
21. Mc Naught, C.E. and Macfie, J. (2001): Probiotics in clinical practice: a critical review of the evidence. Nutr. Res. 21: 343– 353.
22. Messi, P., Bondi, M., Sabia, C., Battini, R. and Manicardi, G. (2001): Detection and preliminary characterization of a bacteriocin (plantaricin 35d) produced by a Lactobacillus plantarum strain. Int. J. Food Microbiol. 64: 193–198.
23. Millette, M., Le Tien, C., Smoragiewicz, W. and Lacroix, M. (2007): Inhibition of Staphylococcus aureus on beef by nisin-containing modiWed alginate Wlms and beads. Food Control 18: 878–884.
24. Naimushin, A. N., Soelberg, S. D., Nguyen, D. K., Dunlap, L., Bartholomew, D., Elkind, J., Melendez, J.and Furlong, C. E. (2002): Detection of Staphylococcus aureus enterotoxin B at femtomolar levels with a miniature integrated two-channel surface plasmon resonance (SPR) sensor. Biosensors and Bioelectronics 17: 573-/584.
25. Noriega, L., Gueimonde, M., Alonso, L. and De Los Reyes-Gavilan C. G. (2003): Inhibition of Bacillus cereus growth in carbonated fermented bifidus milk. Food Microbiol. 20: 519–526.
26. Orrhage, K. and Nord, C.E. (2000): Bifidobacteria and lactobacilli in human health. Drugs Exp. Clin. Res. 26: 95–111.
27. Rosenquist, H., Smidt, L., Andersen, S. R., Jensen, G. B. and Wilcks, A. (2005): Occurrence and significance of Bacillus cereus and Bacillus thuringiensis in ready-to-eat food. FEMS Microbiol. Let. 250: 129–136
28. Rossland, E., Borge, G. I. A., Langsrud, T. and Sorhaug T. (2003): Inhibition of Bacillus cereus by strains of Lactobacillus and Lactococcus in milk. Int. J. Food Microbiol. 89: 205– 212.
29. Rossland, E., Langsrud, T., Granum, P. E. and Sbrhaug, T. (2005): Production of antimicrobial metabolites by strains of Lactobacillus or Lactococcus co-cultured with Bacillus cereus in milk. Int. J. Food Microbiol. 98: 193– 200.
30. Servin, A. (2004): Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev. 28: 405–440.
31. Svensson, B., Monthan, A., Shaheen, R., Andersson, M. A., Salkinoja-Salonen, M. and Christiansson, A. (2006): Occurrence of emetic toxin producing Bacillus cereus in the dairy production chain. Int. Dairy J. 16: 740–749.
32. Topisirovic, L., Kojic, M., Fira, D., Golic, N., Strahinic, I. and Lozo, J. (2006): Potential of lactic acid bacteria isolated from specific natural niches in food production and preservation. Int. J. Food Microbiol. 112: 230–235.
Published
2024-12-09
How to Cite
Choukri TEFIANI, Djilali BENABDELMOUMENE, Abdelmalek CHAALEL, Nawal BOUKEZZOULA, Mimoune SOUNA, Ghada LAMRAOUI, Bahia MEROUFEL, Mohamed Amine ZENASNI, & Ali RIAZI. (2024). Antimicrobial Activity Of Bifidobacterial Cells And Supernatant Against B. Cereus ATCC 9884. Revista Electronica De Veterinaria, 25(2), 626-634. https://doi.org/10.69980/redvet.v25i2.1464
Section
Articles
