Skip to main content
Applied and Environmental Microbiology logoLink to Applied and Environmental Microbiology
. 1997 Jul;63(7):2747–2753. doi: 10.1128/aem.63.7.2747-2753.1997

The human Lactobacillus acidophilus strain LA1 secretes a nonbacteriocin antibacterial substance(s) active in vitro and in vivo.

M F Bernet-Camard 1, V Liévin 1, D Brassart 1, J R Neeser 1, A L Servin 1, S Hudault 1
PMCID: PMC168570  PMID: 9212421

Abstract

The adhering human Lactobacillus acidophilus strain LA1 inhibits the cell association and cell invasion of enteropathogens in cultured human intestinal Caco-2 cells (M. F. Bernet, D. Brassard, J. R. Neeser, and A. L. Servin, Gut 35:483-489, 1994). Here, we demonstrate that strain LA1 developed its antibacterial activity in conventional or germ-free mouse models orally infected by Salmonella typhimurium. We present evidence that the spent culture supernatant of strain LA1 (LA1-SCS) contained antibacterial components active against S. typhimurium infecting the cultured human intestinal Caco-2 cells. The LA1-SCS antibacterial activity was observed in vitro against a wide range of gram-negative and gram-positive pathogens, such as Staphylococcus aureus, Listeria monocytogenes, S. typhimurium, Shigella flexneri, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Enterobacter cloacae. By contrast, no activity was observed against species of the normal gut flora, such as lactobacilli and bifidobacteria. The LA1-SCS antibacterial activity was insensitive to proteases and independent of lactic acid production.

Full Text

The Full Text of this article is available as a PDF (203.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bernet M. F., Brassart D., Neeser J. R., Servin A. L. Lactobacillus acidophilus LA 1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut. 1994 Apr;35(4):483–489. doi: 10.1136/gut.35.4.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blomberg L., Henriksson A., Conway P. L. Inhibition of adhesion of Escherichia coli K88 to piglet ileal mucus by Lactobacillus spp. Appl Environ Microbiol. 1993 Jan;59(1):34–39. doi: 10.1128/aem.59.1.34-39.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bovee-Oudenhoven I., Termont D., Dekker R., Van der Meer R. Calcium in milk and fermentation by yoghurt bacteria increase the resistance of rats to Salmonella infection. Gut. 1996 Jan;38(1):59–65. doi: 10.1136/gut.38.1.59. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chan R. C., Reid G., Irvin R. T., Bruce A. W., Costerton J. W. Competitive exclusion of uropathogens from human uroepithelial cells by Lactobacillus whole cells and cell wall fragments. Infect Immun. 1985 Jan;47(1):84–89. doi: 10.1128/iai.47.1.84-89.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chauvière G., Coconnier M. H., Kerneis S., Darfeuille-Michaud A., Joly B., Servin A. L. Competitive exclusion of diarrheagenic Escherichia coli (ETEC) from human enterocyte-like Caco-2 cells by heat-killed Lactobacillus. FEMS Microbiol Lett. 1992 Mar 15;70(3):213–217. doi: 10.1016/0378-1097(92)90700-x. [DOI] [PubMed] [Google Scholar]
  6. Chauvière G., Coconnier M. H., Kernéis S., Fourniat J., Servin A. L. Adhesion of human Lactobacillus acidophilus strain LB to human enterocyte-like Caco-2 cells. J Gen Microbiol. 1992 Aug;138(Pt 8):1689–1696. doi: 10.1099/00221287-138-8-1689. [DOI] [PubMed] [Google Scholar]
  7. Coconnier M. H., Bernet M. F., Kernéis S., Chauvière G., Fourniat J., Servin A. L. Inhibition of adhesion of enteroinvasive pathogens to human intestinal Caco-2 cells by Lactobacillus acidophilus strain LB decreases bacterial invasion. FEMS Microbiol Lett. 1993 Jul 1;110(3):299–305. doi: 10.1111/j.1574-6968.1993.tb06339.x. [DOI] [PubMed] [Google Scholar]
  8. Coconnier M. H., Klaenhammer T. R., Kernéis S., Bernet M. F., Servin A. L. Protein-mediated adhesion of Lactobacillus acidophilus BG2FO4 on human enterocyte and mucus-secreting cell lines in culture. Appl Environ Microbiol. 1992 Jun;58(6):2034–2039. doi: 10.1128/aem.58.6.2034-2039.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Finlay B. B., Falkow S. Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J Infect Dis. 1990 Nov;162(5):1096–1106. doi: 10.1093/infdis/162.5.1096. [DOI] [PubMed] [Google Scholar]
  10. Fogh J., Fogh J. M., Orfeo T. One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. J Natl Cancer Inst. 1977 Jul;59(1):221–226. doi: 10.1093/jnci/59.1.221. [DOI] [PubMed] [Google Scholar]
  11. Fourniat J., Djaballi Z., Maccario J., Bourlioux P., German A. Influence de l'administration de Lactobacillus acidophilus tués sur la survie de souriceaux infectés avec une souche de Escherichia coli entérotoxinogène. Ann Rech Vet. 1986;17(4):401–407. [PubMed] [Google Scholar]
  12. Goldin B. R., Gorbach S. L., Saxelin M., Barakat S., Gualtieri L., Salminen S. Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig Dis Sci. 1992 Jan;37(1):121–128. doi: 10.1007/BF01308354. [DOI] [PubMed] [Google Scholar]
  13. Gotteland M., Pochart P., Dabbech M., Bisetti N., Desjeux J. F. In vivo effect of yogurt on excretion of enteropathogen Escherichia coli RDEC-1 during acute diarrhea in the just-weaned rabbit. J Pediatr Gastroenterol Nutr. 1992 Apr;14(3):264–267. doi: 10.1097/00005176-199204000-00005. [DOI] [PubMed] [Google Scholar]
  14. Greene J. D., Klaenhammer T. R. Factors involved in adherence of lactobacilli to human Caco-2 cells. Appl Environ Microbiol. 1994 Dec;60(12):4487–4494. doi: 10.1128/aem.60.12.4487-4494.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hamdan I. Y., Mikolajcik E. M. Acidolin: an antibiotic produced by Lactobacillus acidophilus. J Antibiot (Tokyo) 1974 Aug;27(8):631–636. doi: 10.7164/antibiotics.27.631. [DOI] [PubMed] [Google Scholar]
  16. Henriksson A., Szewzyk R., Conway P. L. Characteristics of the adhesive determinants of Lactobacillus fermentum 104. Appl Environ Microbiol. 1991 Feb;57(2):499–502. doi: 10.1128/aem.57.2.499-502.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hitchins A. D., McDonough F. E. Prophylactic and therapeutic aspects of fermented milk. Am J Clin Nutr. 1989 Apr;49(4):675–684. doi: 10.1093/ajcn/49.4.675. [DOI] [PubMed] [Google Scholar]
  18. Hudault S., Liévin V., Bernet-Camard M. F., Servin A. L. Antagonistic activity exerted in vitro and in vivo by Lactobacillus casei (strain GG) against Salmonella typhimurium C5 infection. Appl Environ Microbiol. 1997 Feb;63(2):513–518. doi: 10.1128/aem.63.2.513-518.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Isberg R. R., Leong J. M. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell. 1990 Mar 9;60(5):861–871. doi: 10.1016/0092-8674(90)90099-z. [DOI] [PubMed] [Google Scholar]
  20. Isolauri E., Juntunen M., Rautanen T., Sillanaukee P., Koivula T. A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. Pediatrics. 1991 Jul;88(1):90–97. [PubMed] [Google Scholar]
  21. Isolauri E., Kaila M., Mykkänen H., Ling W. H., Salminen S. Oral bacteriotherapy for viral gastroenteritis. Dig Dis Sci. 1994 Dec;39(12):2595–2600. doi: 10.1007/BF02087695. [DOI] [PubMed] [Google Scholar]
  22. Jack R. W., Tagg J. R., Ray B. Bacteriocins of gram-positive bacteria. Microbiol Rev. 1995 Jun;59(2):171–200. doi: 10.1128/mr.59.2.171-200.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kaila M., Isolauri E., Soppi E., Virtanen E., Laine S., Arvilommi H. Enhancement of the circulating antibody secreting cell response in human diarrhea by a human Lactobacillus strain. Pediatr Res. 1992 Aug;32(2):141–144. doi: 10.1203/00006450-199208000-00002. [DOI] [PubMed] [Google Scholar]
  24. Klaenhammer T. R. Genetics of bacteriocins produced by lactic acid bacteria. FEMS Microbiol Rev. 1993 Sep;12(1-3):39–85. doi: 10.1111/j.1574-6976.1993.tb00012.x. [DOI] [PubMed] [Google Scholar]
  25. Klinkert M. Q., Herrmann R., Schaller H. Surface proteins of Mycoplasma hyopneumoniae identified from an Escherichia coli expression plasmid library. Infect Immun. 1985 Aug;49(2):329–335. doi: 10.1128/iai.49.2.329-335.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lehrer R. I., Rosenman M., Harwig S. S., Jackson R., Eisenhauer P. Ultrasensitive assays for endogenous antimicrobial polypeptides. J Immunol Methods. 1991 Mar 21;137(2):167–173. doi: 10.1016/0022-1759(91)90021-7. [DOI] [PubMed] [Google Scholar]
  27. Link-Amster H., Rochat F., Saudan K. Y., Mignot O., Aeschlimann J. M. Modulation of a specific humoral immune response and changes in intestinal flora mediated through fermented milk intake. FEMS Immunol Med Microbiol. 1994 Nov;10(1):55–63. doi: 10.1111/j.1574-695X.1994.tb00011.x. [DOI] [PubMed] [Google Scholar]
  28. Livrelli V., De Champs C., Di Martino P., Darfeuille-Michaud A., Forestier C., Joly B. Adhesive properties and antibiotic resistance of Klebsiella, Enterobacter, and Serratia clinical isolates involved in nosocomial infections. J Clin Microbiol. 1996 Aug;34(8):1963–1969. doi: 10.1128/jcm.34.8.1963-1969.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Marteau P., Pochart P., Flourié B., Pellier P., Santos L., Desjeux J. F., Rambaud J. C. Effect of chronic ingestion of a fermented dairy product containing Lactobacillus acidophilus and Bifidobacterium bifidum on metabolic activities of the colonic flora in humans. Am J Clin Nutr. 1990 Oct;52(4):685–688. doi: 10.1093/ajcn/52.4.685. [DOI] [PubMed] [Google Scholar]
  30. Marteau P., Rambaud J. C. Potential of using lactic acid bacteria for therapy and immunomodulation in man. FEMS Microbiol Rev. 1993 Sep;12(1-3):207–220. doi: 10.1111/j.1574-6976.1993.tb00019.x. [DOI] [PubMed] [Google Scholar]
  31. McGroarty J. A., Reid G. Detection of a Lactobacillus substance that inhibits Escherichia coli. Can J Microbiol. 1988 Aug;34(8):974–978. doi: 10.1139/m88-171. [DOI] [PubMed] [Google Scholar]
  32. Moyen E. N., Bonneville F., Fauchère J. L. Modification par l'érythromycine et un extrait de Lactobacillus acidophilus de la colonisation de l'intestin et de la translocation de Campylobacter jejuni chez la souris axénique. Ann Inst Pasteur Microbiol. 1986 Mar-Apr;137A(2):199–207. doi: 10.1016/s0769-2609(86)80024-2. [DOI] [PubMed] [Google Scholar]
  33. Ouwehand A. C., Conway P. L. Purification and characterization of a component produced by Lactobacillus fermentum that inhibits the adhesion of K88 expressing Escherichia coli to porcine ileal mucus. J Appl Bacteriol. 1996 Mar;80(3):311–318. doi: 10.1111/j.1365-2672.1996.tb03225.x. [DOI] [PubMed] [Google Scholar]
  34. Pardon P., Popoff M. Y., Coynault C., Marly J., Miras I. Virulence-associated plasmids of Salmonella serotype Typhimurium in experimental murine infection. Ann Inst Pasteur Microbiol. 1986 Jul-Aug;137B(1):47–60. doi: 10.1016/s0769-2609(86)80093-x. [DOI] [PubMed] [Google Scholar]
  35. Pedrosa M. C., Golner B. B., Goldin B. R., Barakat S., Dallal G. E., Russell R. M. Survival of yogurt-containing organisms and Lactobacillus gasseri (ADH) and their effect on bacterial enzyme activity in the gastrointestinal tract of healthy and hypochlorhydric elderly subjects. Am J Clin Nutr. 1995 Feb;61(2):353–359. doi: 10.1093/ajcn/61.2.353. [DOI] [PubMed] [Google Scholar]
  36. Salomón R. A., Farías R. N. Microcin 25, a novel antimicrobial peptide produced by Escherichia coli. J Bacteriol. 1992 Nov;174(22):7428–7435. doi: 10.1128/jb.174.22.7428-7435.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sanders M. E. Summary of conclusions from a consensus panel of experts on health attributes of lactic cultures: significance to fluid milk products containing cultures. J Dairy Sci. 1993 Jul;76(7):1819–1828. doi: 10.3168/jds.S0022-0302(93)77514-1. [DOI] [PubMed] [Google Scholar]
  38. Schiffrin E. J., Rochat F., Link-Amster H., Aeschlimann J. M., Donnet-Hughes A. Immunomodulation of human blood cells following the ingestion of lactic acid bacteria. J Dairy Sci. 1995 Mar;78(3):491–497. doi: 10.3168/jds.S0022-0302(95)76659-0. [DOI] [PubMed] [Google Scholar]
  39. Silva M., Jacobus N. V., Deneke C., Gorbach S. L. Antimicrobial substance from a human Lactobacillus strain. Antimicrob Agents Chemother. 1987 Aug;31(8):1231–1233. doi: 10.1128/aac.31.8.1231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Talarico T. L., Dobrogosz W. J. Chemical characterization of an antimicrobial substance produced by Lactobacillus reuteri. Antimicrob Agents Chemother. 1989 May;33(5):674–679. doi: 10.1128/aac.33.5.674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. VINCENT J. G., VEOMETT R. C., RILEY R. F. Antibacterial activity associated with Lactobacillus acidophilus. J Bacteriol. 1959 Oct;78:477–484. doi: 10.1128/jb.78.4.477-484.1959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Velraeds M. M., van der Mei H. C., Reid G., Busscher H. J. Inhibition of initial adhesion of uropathogenic Enterococcus faecalis by biosurfactants from Lactobacillus isolates. Appl Environ Microbiol. 1996 Jun;62(6):1958–1963. doi: 10.1128/aem.62.6.1958-1963.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Vescovo M., Scolari G. L., Caravaggi L., Bottazzi V. Antimicrobial compounds from Lactobacillus casei and Lactobacillus helveticus. New Microbiol. 1993 Apr;16(2):171–175. [PubMed] [Google Scholar]

Articles from Applied and Environmental Microbiology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES