Chromosomal genes-mediated inhibition of intestinal and foodborne pathogens by Lactobacillus acidophilus AA11

Aly E. Abo-Amer

2006, Number 1

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Microbiología 2006; 48 (1)

Chromosomal genes-mediated inhibition of intestinal and foodborne pathogens by Lactobacillus acidophilus AA11

Abo-Amer AE

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Language: English
References: 97
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ABSTRACT

Approximately 63 strains of Lactobacillus acidophilus were isolated from Egyptian home-made cheese and examined for production of antagonism. Only eight strains demonstrated inhibitory activity against spoilage microorganisms (i.e. Staphylococcus aureus and Bacillus cereus) and pathogens (i.e. E. coli, Salmonella sp. and Shigella sp.). Lactobacillus acidophilus AA11 produced a more antimicrobial activity with a wide range of inhibition. The agent AA11 was sensitive to proteolytic enzymes and retained full activity after 30 min at 100 oC. Activity against sensitive cells was bactericidal but not bacteriolytic. The compound was produced during growth phase and can be extracted from the culture supernatant fluids with n-Butanol. 12 % SDS-PAGE analysis of 40% ammonium sulphate precipitated agent showed two peptides with molecular weights of ~36 kDa and ~29 kDa. No plasmid was identified in Lactobacillus acidophilus AA11 indicating that the genes encoding the inhibitory agent located on the chromosome. These characteristics identify the inhibitory substance as a bacteriocin, designated acidocin AA11 and confer the agent an application potential as a biopreservative.

REFERENCES

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Barefoot, S.F. and Klaenhammer, T. R. 1984. Purification and characterization of the Lactobacillus acidophilus bacteriocins, lactacin B. Antimicrobial Agents and Chemotherapy 26:328-334.
Bergey’s Manual of Systematic Bacteriology, 1984. N. Krieg (Ed), vol. 1, 2, Baltimore: Williams and Wilkins.
Bourlioux, P. 1997. What is currently known about the molecular mechanisms of colonization resistance? Anaerobe 3:179-184.
Chen, H. and Hoover, D.G., 2003. Bacteriocins and their food applications. Comprehensive Rev. Food Sci. Food Safety 2:82-100.
Cuozzo, S. A., Sesma, F., Palacios, J. M., Holgado, A. P. D., & Raya, R. R. 2000. Identification and nucleotide sequence of genes involved in the synthesis of lactocin 705, a two-peptide bacteriocin from Lactobacillus casei CRL 705. FEMS Microbiol. Lett. 185:157-161.
De Klerk, H. C., and Coetzee, J. N. 1961. Antibiosis among lactobacilli. Nature 192:340-341.
De Klerk, H. C., and Smit, J. A. 1967. Properties of a Lactobacillus fermenti bacteriocin. J. Gen. Microbiol. 48:309-316.
De Man, J. C., Rogosa, M. E. and Sharpe, M. E. 1960. A medium for the cultivation of Lactobacilli. J. Appl. Bacteriol. 23:130-135.
De Vuyst, L. and Vandamme, E. J. 1994. Bacteriocins of Lactic Acid Bacteria: Microbiology, Genetics and Applications, Blackie Academic and Professional, London.
Deraz, S. F., Karlsson, E. N., Hedstrom, M., Andersson, M. M. and Mattiasson, B. 2005. Purification and characterization of acidocin D20079, a bacteriocin produced by Lactobacillus acidophilus DSM 20079. J. Biotech. 117:343-354.
Fleming, H. P., Etchells, J. L. and Costilow, R. L. 1975. Microbial inhibition by an isolate of Pediococcus from cucumber brines. Appl. Microbiol. 30:1040-1042.
Fooks, L. J. and Gibson, G. R. 2002. In vitro investigations of the effect of probiotics and prebiotics on selected human intestinal pathogens. FEMS Microbiol. Ecol. 39:67-75.
Gilliland, S. E., and Speck, M. L. 1977. Use of the Minitek system for characterizing lactobacilli. Appl. Environ. Microbiol. 6:1289-1292.
Hamdan, I. Y, and Mikolajcik, E. M. 1974. Acidolin: an antibiotic produced by Lactobacillus acidophilus. J. Antibiot. (Tokyo). 27:631-636.
Hosono, A., Yastuki, K. and Tokita, F. 1977. Isolation and characterization of an inhibitory substance against Escherichia coli produced by Lactobacillus acidophilus. Milchwissenschaft 32:727-730.
Hurst, A. 1973. Microbial antagonism in foods. Can. Inst. Food Sci. Technol. J. 6:80-90.
Jack, R.W., Tagg, J. R. and Ray, B. 1995. Bacteriocins of Gram-positive bacteria. Microbiol. Rev. 59:171–200.
Kanatania, K., Tahara, T., Yoshida, K., Miura, H., Sakamoto, M. and Oshimura, M. 1992. Plasmid-associated bacteriocin production by and immunity of Lactobacillus acidophilus TK8912. Biosci. Biotech. Biochem. 56:648-651.
Kawai, Y., Saitoh, B., Takahashi, O., Kitazawa, H., Saito, T., Nakajima, H. and Itoh, T. 2000. Primary amino acid and DNA sequences ofgassericin T, a lactacin F-family bacteriocin produced by Lactobacillus gasseri SBT2055. Biosci. Biotech. Biochem. 64:2201-2208.
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Klaenhammer, T. R. 1982. Microbiological considerations in selection and preparation of Lactobacillus strains for uses as dietary adjuncts. J. Dairy Sci. 65:1339-1349.
Klaenhammer, T. R. 1993. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev. 12:39-86.
Klaenhammer, T. R., and Kullen, M. J. 1999. Selection and design of probiotics. International J. Food Microbiol. 50:45-57.
Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
Metchnikoof, E. 1908. The prolongation of life. G.P. Putnam’s Sons, New York.
Morin, A., Saheb, S. A., Bisaillon, J. G., Beaudet, R. and Sylvestre, M. 1980. Effect of culture medium composition on inhibition of growth of Neisseria gonorrhoeae by lactobacilli. Curr. Microbiol. 4:283-286.
Muriana, P. M. and Kleanhammer, T. R. 1987. Conjugal transfer of plasmid encoded determinants for bacteriocin production and immunity in Lactobacillus acidophilus 88. Appl. Environ. Microbiol. 53:553-560.
Muriana, P. M. and Kleanhammer, T. R. 1991. Purification and partial characterization of lactacin F, a bacteriocin produced by Lactobacillus acidophilus 11088. Appl. Environ. Microbiol. 57:114-121.
Naidu, A. S., Bidlack, W. R., Clemens, R. A. 1999. Probiotic spectra of lactic acid bacteria (LAB). Crit. Rev. Food Sci. Nutrition 38:13-126.
Ouwehand, A. C., Kirjavainen, P. V., Shortt, C., and Salminen, S. 1999. Probiotics: mechanisms and established effects. Int. Dairy J. 9:43-52.
Piard, J.C. and Desmazeaud, M. 1992. Inhibiting factors produced by lactic acid bacteria. Part 2. Bacteriocins and other antibacterial substances. Lait 72:113-142.
Reid, G., Howard, J., and Gan, B. S. 2001. Can bacterial interference prevent infection? Trends in Microbiol. 9:424-428.
Salminen, S., Isolauri, E., and Salminen, E. 1996. Clinical uses of probiotics for stabilizing the gut mucosal barrier: successful strains and future challenges. Antonie Van Leeuwenhoek Int. J. G. Mol. Microbiol. 70:347-358.
Sambrook, J., Fritsch, E. F. and Maniatis, T. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
Shahani, K. M., and Ayebo, A. D. 1980. Role of dietary lactobacilli in gastrointestinal microecology. Am. J. Clin. Nutr. 33:2448-2457.
Tag, J.R. and McGiven, A.R. 1971. Assay system for bacteriocin. Appl. Microbiol. 21:943.
Tagg, J.R., Dajani, A.S., and Wannamaker, L.W. 1976. Bacteriocins of gram-positive bacteria. Bacteriol. Rev. 40:722-756.
Tahar, T., Kanatania, K., Yoshida, K., Miura, H. Sakamoto, M. and Oshimura, M. 1992. Purification and some properties of acidocin 8912, a novel bacteriocin produced by Lactobacillus acidophilus TK8912. Biosci. Biotech. Biochem. 56:1212-1215.
ten Brink, B., Minekus, M, van der Vossen, J.M.B.M., Leer, R. J. and Huis in’t Veld, J. H. J. 1994. Antimicrobial activity of lactobacilli: preliminary characterization and optimization of production of acidocin B, a novel bacteriocin produced by Lactobacillus acidophilus M46. J. Appli. Bacteriol. 77:140-148.
Toba, T., Yoshioka, E. and Itoh, T. 1991. Acidophilucin A, a new heat-labile bacteriocin produced by Lactobacillus acidophilus LAPT 1060. Lett. in Appli Microbiol. 12:106-108.
Todorov, S. D. and Dicks, L. M. T. 2005. Effect of Growth Medium on Bacteriocin Production by Lactobacillus plantarum ST194BZ, a Strain Isolated from Boza. Food Technol.
Biotechnol. 43:165-173.
Tramer, J. 1966. Inhibitory effect of Lactobacillus acidophilus. Nature. 211:204-205.
Upreti, G. C, and Hinsdill, R. D. 1973. Isolation and Characterization of a bacteriocin from a Homofermentative Lactobacillus. Antimicrob Agents Chemother. 4:487-494.
Upreti, G. C. and Hinsdill, R. D. 1975. Production and Mode of Action of Lactocin 27: Bacteriocin from a Homofermentative Lactobacillus. Antimicrob Agents Chemother. 7:139-145.
Vincent, J. G., Veomett, R. C., and Riley, R. F. 1959. Antibacterial activity associated with Lactobacillus acidophilus. J. Bacteriol. 78:477-484.
Zamfir, M., Callewaert, R., Cornea, P. C., Savu, L., Vatafu, I., and De Vuyst, L. 1999. Purification and characterization of a bacteriocin produced by Lactobacillus acidophilus IBB 801. J. Appl. Microbiol. 87:923-931.
Aymerich, M.T., Garriga, M., Monfort, J.M., Nes, I., Hugas, M., 2000. Bacteriocin-producing Lactobacilli in Spanish-style fermented sausages: characterization of bacteriocins. Food Microbiol. 17:33-45.
Barefoot, S. F. and Klaenhammer, T. R. 1983. Detection and activity of lactacin B, a bacteriocin produced by Lactobacillus acidophilus. Appl. Environ. Microbiol. 45:1808-1815.
Barefoot, S.F. and Klaenhammer, T. R. 1984. Purification and characterization of the Lactobacillus acidophilus bacteriocins, lactacin B. Antimicrobial Agents and Chemotherapy 26:328-334.
Bergey’s Manual of Systematic Bacteriology, 1984. N. Krieg (Ed), vol. 1, 2, Baltimore: Williams and Wilkins.
Bourlioux, P. 1997. What is currently known about the molecular mechanisms of colonization resistance? Anaerobe 3:179-184.
Chen, H. and Hoover, D.G., 2003. Bacteriocins and their food applications. Comprehensive Rev. Food Sci. Food Safety 2:82-100.
Cuozzo, S. A., Sesma, F., Palacios, J. M., Holgado, A. P. D., & Raya, R. R. 2000. Identification and nucleotide sequence of genes involved in the synthesis of lactocin 705, a two-peptide bacteriocin from Lactobacillus casei CRL 705. FEMS Microbiol. Lett. 185:157-161.
De Klerk, H. C., and Coetzee, J. N. 1961. Antibiosis among lactobacilli. Nature 192:340-341.
De Klerk, H. C., and Smit, J. A. 1967. Properties of a Lactobacillus fermenti bacteriocin. J. Gen. Microbiol. 48:309-316.
De Man, J. C., Rogosa, M. E. and Sharpe, M. E. 1960. A medium for the cultivation of Lactobacilli. J. Appl. Bacteriol. 23:130-135.
De Vuyst, L. and Vandamme, E. J. 1994. Bacteriocins of Lactic Acid Bacteria: Microbiology, Genetics and Applications, Blackie Academic and Professional, London.
Deraz, S. F., Karlsson, E. N., Hedstrom, M., Andersson, M. M. and Mattiasson, B. 2005. Purification and characterization of acidocin D20079, a bacteriocin produced by Lactobacillus acidophilus DSM 20079. J. Biotech. 117:343-354.
Fleming, H. P., Etchells, J. L. and Costilow, R. L. 1975. Microbial inhibition by an isolate of Pediococcus from cucumber brines. Appl. Microbiol. 30:1040-1042.
Fooks, L. J. and Gibson, G. R. 2002. In vitro investigations of the effect of probiotics and prebiotics on selected human intestinal pathogens. FEMS Microbiol. Ecol. 39:67-75.
Gilliland, S. E., and Speck, M. L. 1977. Use of the Minitek system for characterizing lactobacilli. Appl. Environ. Microbiol. 6:1289-1292.
Hamdan, I. Y, and Mikolajcik, E. M. 1974. Acidolin: an antibiotic produced by Lactobacillus acidophilus. J. Antibiot. (Tokyo). 27:631-636.
Hosono, A., Yastuki, K. and Tokita, F. 1977. Isolation and characterization of an inhibitory substance against Escherichia coli produced by Lactobacillus acidophilus. Milchwissenschaft 32:727-730.
Hurst, A. 1973. Microbial antagonism in foods. Can. Inst. Food Sci. Technol. J. 6:80-90.
Jack, R.W., Tagg, J. R. and Ray, B. 1995. Bacteriocins of Gram-positive bacteria. Microbiol. Rev. 59:171–200.
Kanatania, K., Tahara, T., Yoshida, K., Miura, H., Sakamoto, M. and Oshimura, M. 1992. Plasmid-associated bacteriocin production by and immunity of Lactobacillus acidophilus TK8912. Biosci. Biotech. Biochem. 56:648-651.
Kawai, Y., Saitoh, B., Takahashi, O., Kitazawa, H., Saito, T., Nakajima, H. and Itoh, T. 2000. Primary amino acid and DNA sequences ofgassericin T, a lactacin F-family bacteriocin produced by Lactobacillus gasseri SBT2055. Biosci. Biotech. Biochem. 64:2201-2208.
Kitazawa, H., Ino, T., Kawai, Y., Itoh, T., Saito, T., 2002. A novel immunostimulating aspect of Lactobacillus gasseri: induction of ‘Gasserokine’ as chemoattractants for macrophages. Int. J. Food Microbiol. 77:29-38.
Klaenhammer, T. R. 1982. Microbiological considerations in selection and preparation of Lactobacillus strains for uses as dietary adjuncts. J. Dairy Sci. 65:1339-1349.
Klaenhammer, T. R. 1993. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol. Rev. 12:39-86.
Klaenhammer, T. R., and Kullen, M. J. 1999. Selection and design of probiotics. International J. Food Microbiol. 50:45-57.
Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
Metchnikoof, E. 1908. The prolongation of life. G.P. Putnam’s Sons, New York.
Morin, A., Saheb, S. A., Bisaillon, J. G., Beaudet, R. and Sylvestre, M. 1980. Effect of culture medium composition on inhibition of growth of Neisseria gonorrhoeae by lactobacilli. Curr. Microbiol. 4:283-286.
Muriana, P. M. and Kleanhammer, T. R. 1987. Conjugal transfer of plasmid encoded determinants for bacteriocin production and immunity in Lactobacillus acidophilus 88. Appl. Environ. Microbiol. 53:553-560.
Muriana, P. M. and Kleanhammer, T. R. 1991. Purification and partial characterization of lactacin F, a bacteriocin produced by Lactobacillus acidophilus 11088. Appl. Environ. Microbiol. 57:114-121.
Naidu, A. S., Bidlack, W. R., Clemens, R. A. 1999. Probiotic spectra of lactic acid bacteria (LAB). Crit. Rev. Food Sci. Nutrition 38:13-126.
Ouwehand, A. C., Kirjavainen, P. V., Shortt, C., and Salminen, S. 1999. Probiotics: mechanisms and established effects. Int. Dairy J. 9:43-52.
Piard, J.C. and Desmazeaud, M. 1992. Inhibiting factors produced by lactic acid bacteria. Part 2. Bacteriocins and other antibacterial substances. Lait 72:113-142.
Reid, G., Howard, J., and Gan, B. S. 2001. Can bacterial interference prevent infection? Trends in Microbiol. 9:424-428.
Salminen, S., Isolauri, E., and Salminen, E. 1996. Clinical uses of probiotics for stabilizing the gut mucosal barrier: successful strains and future challenges. Antonie Van Leeuwenhoek Int. J. G. Mol. Microbiol. 70:347-358.
Sambrook, J., Fritsch, E. F. and Maniatis, T. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
Shahani, K. M., and Ayebo, A. D. 1980. Role of dietary lactobacilli in gastrointestinal microecology. Am. J. Clin. Nutr. 33:2448-2457.
Tag, J.R. and McGiven, A.R. 1971. Assay system for bacteriocin. Appl. Microbiol. 21:943.
Tagg, J.R., Dajani, A.S., and Wannamaker, L.W. 1976. Bacteriocins of gram-positive bacteria. Bacteriol. Rev. 40:722-756.
Tahar, T., Kanatania, K., Yoshida, K., Miura, H. Sakamoto, M. and Oshimura, M. 1992. Purification and some properties of acidocin 8912, a novel bacteriocin produced by Lactobacillus acidophilus TK8912. Biosci. Biotech. Biochem. 56:1212-1215.
ten Brink, B., Minekus, M, van der Vossen, J.M.B.M., Leer, R. J. and Huis in’t Veld, J. H. J. 1994. Antimicrobial activity of lactobacilli: preliminary characterization and optimization of production of acidocin B, a novel bacteriocin produced by Lactobacillus acidophilus M46. J. Appli. Bacteriol. 77:140-148.
Toba, T., Yoshioka, E. and Itoh, T. 1991. Acidophilucin A, a new heat-labile bacteriocin produced by Lactobacillus acidophilus LAPT 1060. Lett. in Appli Microbiol. 12:106-108.
Todorov, S. D. and Dicks, L. M. T. 2005. Effect of Growth Medium on Bacteriocin Production by Lactobacillus plantarum ST194BZ, a Strain Isolated from Boza. Food Technol. Biotechnol. 43:165-173.
Tramer, J. 1966. Inhibitory effect of Lactobacillus acidophilus. Nature. 211:204-205.
Upreti, G. C, and Hinsdill, R. D. 1973. Isolation and Characterization of a bacteriocin from a Homofermentative Lactobacillus. Antimicrob Agents Chemother. 4:487-494.
Upreti, G. C. and Hinsdill, R. D. 1975. Production and Mode of Action of Lactocin 27: Bacteriocin from a Homofermentative Lactobacillus. Antimicrob Agents Chemother. 7:139-145.
Vincent, J. G., Veomett, R. C., and Riley, R. F. 1959. Antibacterial activity associated with Lactobacillus acidophilus. J. Bacteriol. 78:477-484.
Zamfir, M., Callewaert, R., Cornea, P. C., Savu, L., Vatafu, I., and De Vuyst, L. 1999. Purification and characterization of a bacteriocin produced by Lactobacillus acidophilus IBB 801. J. Appl. Microbiol. 87:923-931.