1887

Abstract

New biological strategies for the treatment of infection are needed in response to the increase in antibiotic-resistant strains. L1000 and RBL67 were previously shown to produce antimicrobial proteinaceous compounds (microcin B17 and thermophilicin B67, respectively) active against a panel of strains recently isolated from clinical cases in Switzerland. In this study, two three-stage intestinal continuous fermentation models of colonization inoculated with immobilized faeces of a two-year-old child were implemented to study the effects of the two bacteriocinogenic strains compared with a bacteriocin-negative mutant of strain L1000 on growth, as well as gut microbiota composition and metabolic activity. Immobilized L1000 added to the proximal colon reactor showed a low colonization, and developed preferentially in the distal colon reactor independent of the presence of genetic determinants for microcin B17 production. Surprisingly, L1000 addition strongly stimulated growth in all three reactors. In contrast, RBL67 added in a second phase stabilized at high levels in all reactors, but could not inhibit already present at a high level (>10 c.f.u. ml) when the probiotic was added. Inulin added at the end of fermentation induced a strong bifidogenic effect in all three colon reactors and a significant increase of counts in the distal colon reactor. Our data show that under the simulated child colonic conditions, the microcin B17 production phenotype does not correlate with inhibition of but leads to a better colonization of L1000 in the distal colon reactor. We conclude that models with complex and complete gut microbiota are required to accurately assess the potential and efficacy of probiotics with respect to colonization in the gut.

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2010-11-01
2019-11-17
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References

  1. Barth, S., Duncker, S., Hempe, J., Breves, G., Baljer, G. & Bauerfeind, R. ( 2009; ). Escherichia coli Nissle 1917 for probiotic use in piglets: evidence for intestinal colonization. J Appl Microbiol 107, 1697–1710.[CrossRef]
    [Google Scholar]
  2. Bartosch, S., Fite, A., Macfarlane, G. T. & McMurdo, M. E. ( 2004; ). Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol 70, 3575–3581.[CrossRef]
    [Google Scholar]
  3. Basu, S., Paul, D. K., Ganguly, S., Chatterjee, M. & Chandra, P. K. ( 2009; ). Efficacy of high-dose Lactobacillus rhamnosus GG in controlling acute watery diarrhea in Indian children: a randomized controlled trial. J Clin Gastroenterol 43, 208–213.[CrossRef]
    [Google Scholar]
  4. Bovee-Oudenhoven, I. M., ten Bruggencate, S. J., Lettink-Wissink, M. L. & van der Meer, R. ( 2003; ). Dietary fructo-oligosaccharides and lactulose inhibit intestinal colonisation but stimulate translocation of Salmonella in rats. Gut 52, 1572–1578.[CrossRef]
    [Google Scholar]
  5. Cinquin, C., Le Blay, G., Fliss, I. & Lacroix, C. ( 2006; ). New three-stage in vitro model for infant colonic fermentation with immobilized fecal microbiota. FEMS Microbiol Ecol 57, 324–336.[CrossRef]
    [Google Scholar]
  6. Cleusix, V., Lacroix, C., Vollenweider, S. & Le Blay, G. ( 2008; ). Glycerol induces reuterin production and decreases Escherichia coli population in an in vitro model of colonic fermentation with immobilized human feces. FEMS Microbiol Ecol 63, 56–64.[CrossRef]
    [Google Scholar]
  7. Cleusix, V., Lacroix, C., Dasen, G., Leo, M. & Le Blay, G. ( 2010; ). Comparative study of a new quantitative real-time PCR targeting the xylulose-5-phosphate/fructose-6-phosphate phosphoketolase bifidobacterial gene (xfp) in faecal samples with two fluorescence in situ hybridization methods. J Appl Microbiol 108, 181–193.[CrossRef]
    [Google Scholar]
  8. Collado, M. C., Isolauri, E., Salminen, S. & Sanz, Y. ( 2009; ). The impact of probiotic on gut health. Curr Drug Metab 10, 68–78.[CrossRef]
    [Google Scholar]
  9. Corr, S. C., Li, Y., Riedel, C. U., O'Toole, P. W., Hill, C. & Gahan, C. G. ( 2007; ). Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc Natl Acad Sci U S A 104, 7617–7621.[CrossRef]
    [Google Scholar]
  10. Corr, S. C., Hill, C. & Gahan, C. G. ( 2009; ). Understanding the mechanisms by which probiotics inhibit gastrointestinal pathogens. Adv Food Nutr Res 56, 1–15.
    [Google Scholar]
  11. Crum-Cianflone, N. F. ( 2008; ). Salmonellosis and the gastrointestinal tract: more than just peanut butter. Curr Gastroenterol Rep 10, 424–431.[CrossRef]
    [Google Scholar]
  12. Dabour, N., Zihler, A., Kheadr, E., Lacroix, C. & Fliss, I. ( 2009; ). In vivo study on the effectiveness of pediocin PA-1 and Pediococcus acidilactici UL5 at inhibiting Listeria monocytogenes. Int J Food Microbiol 133, 225–233.[CrossRef]
    [Google Scholar]
  13. de Vrese, M. & Schrezenmeir, J. ( 2008; ). Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol 111, 1–66.
    [Google Scholar]
  14. Fallingborg, J., Christensen, L. A., Ingeman-Nielsen, M., Jacobsen, B. A., Abildgaard, K., Rasmussen, H. H. & Rasmussen, S. N. ( 1990; ). Measurement of gastrointestinal pH and regional transit times in normal children. J Pediatr Gastroenterol Nutr 11, 211–214.[CrossRef]
    [Google Scholar]
  15. Furet, J. P., Firmesse, O., Gourmelon, M., Bridonneau, C., Tap, J., Mondot, S., Doré, J. & Corthier, G. ( 2009; ). Comparative assessment of human and farm animal faecal microbiota using real-time quantitative PCR. FEMS Microbiol Ecol 68, 351–362.[CrossRef]
    [Google Scholar]
  16. Gaskins, H. R., Croix, J. A., Nakamura, N. & Nava, G. M. ( 2008; ). Impact of the intestinal microbiota on the development of mucosal defense. Clin Infect Dis 46 (Suppl. 2), S80–S86.[CrossRef]
    [Google Scholar]
  17. Gill, H. & Prasad, J. ( 2008; ). Probiotics, immunomodulation, and health benefits. Adv Exp Med Biol 606, 423–454.
    [Google Scholar]
  18. Guo, X., Xia, X., Tang, R., Zhou, J., Zhao, H. & Wang, K. ( 2008; ). Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs. Lett Appl Microbiol 47, 367–373.[CrossRef]
    [Google Scholar]
  19. Hapfelmeier, S., Ehrbar, K., Stecher, B., Barthel, M., Kremer, M. & Hardt, W. D. ( 2004; ). Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun 72, 795–809.[CrossRef]
    [Google Scholar]
  20. Kheadr, E., Zihler, A., Dabour, N., Lacroix, C., Le Blay, G. & Fliss, I. ( 2010; ). Study of the physicochemical and biological stability of pediocin PA-1 in the upper gastrointestinal tract conditions using a dynamic in vitro model. J Appl Microbiol 109, 54–64.
    [Google Scholar]
  21. Kingsley, R. A., Msefula, C. L., Thomson, N. R., Kariuki, S., Holt, K. E., Gordon, M. A., Harris, D., Clarke, L., Whitehead, S. & other authors ( 2009; ). Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 19, 2279–2287.[CrossRef]
    [Google Scholar]
  22. Kleessen, B., Hartmann, L. & Blaut, M. ( 2001; ). Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human fecal flora. Br J Nutr 86, 291–300.[CrossRef]
    [Google Scholar]
  23. Langlands, S. J., Hopkins, M. J., Coleman, N. & Cummings, J. H. ( 2004; ). Prebiotic carbohydrates modify the mucosa associated microflora of the human large bowel. Gut 53, 1610–1616.[CrossRef]
    [Google Scholar]
  24. Le Blay, G., Rytka, J., Zihler, A. & Lacroix, C. ( 2009; ). New in vitro colonic fermentation model for Salmonella infection in the child gut. FEMS Microbiol Ecol 67, 198–207.[CrossRef]
    [Google Scholar]
  25. Macfarlane, G. T., Macfarlane, S. & Gibson, G. R. ( 1998; ). Validation of a three-stage compound continuous culture system for investigating the effect of retention time on the ecology and metabolism of bacteria in the human colon. Microb Ecol 35, 180–187.[CrossRef]
    [Google Scholar]
  26. Mathys, S., Lacroix, C., Mini, R. & Meile, L. ( 2008; ). PCR and real-time PCR primers developed for detection and identification of Bifidobacterium thermophilum in faeces. BMC Microbiol 8, 179.[CrossRef]
    [Google Scholar]
  27. Michel, C., Kravtchenko, T. P., David, A., Gueneau, S., Kozlowski, F. & Cherbut, C. ( 1998; ). In vitro prebiotic effects of Acacia gums onto the human intestinal microbiota depends on both origin and environmental pH. Anaerobe 4, 257–266.[CrossRef]
    [Google Scholar]
  28. Ohl, M. E. & Miller, S. I. ( 2001; ). Salmonella: a model for bacterial pathogenesis. Annu Rev Med 52, 259–274.[CrossRef]
    [Google Scholar]
  29. Petersen, A., Heegaard, P. M., Pedersen, A. L., Andersen, J. B., Sørensen, R. B., Frøkiaer, H., Lahtinen, S. J., Ouwehand, A. C., Poulsen, M. & Licht, T. R. ( 2009; ). Some putative prebiotics increase the severity of Salmonella enterica serovar Typhimurium infection in mice. BMC Microbiol 9, 245.[CrossRef]
    [Google Scholar]
  30. Pons, A. M., Lanneluc, I., Cottenceau, G. & Sable, S. ( 2002; ). New developments in non-post translationally modified microcins. Biochimie 84, 531–537.[CrossRef]
    [Google Scholar]
  31. Ramirez-Farias, C., Slezak, K., Fuller, Z., Duncan, A., Holtrop, G. & Louis, P. ( 2009; ). Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br J Nutr 101, 541–550.
    [Google Scholar]
  32. Stecher, B. & Hardt, W. D. ( 2008; ). The role of microbiota in infectious disease. Trends Microbiol 16, 107–114.[CrossRef]
    [Google Scholar]
  33. Stecher, B., Chaffron, S., Kappeli, R., Hapfelmeier, S., Freedrich, S., Weber, T. C., Kirundi, J., Suar, M., McCoy, K. D. & other authors ( 2010; ). Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog 6, e1000711.[CrossRef]
    [Google Scholar]
  34. Ten Bruggencate, S. J., Bovee-Oudenhoven, I. M., Lettink-Wissink, M. L. & Van der Meer, R. ( 2003; ). Dietary fructo-oligosaccharides dose-dependently increase translocation of salmonella in rats. J Nutr 133, 2313–2318.
    [Google Scholar]
  35. Ten Bruggencate, S. J., Bovee-Oudenhoven, I. M., Lettink-Wissink, M. L., Katan, M. B. & Van Der Meer, R. ( 2004; ). Dietary fructo-oligosaccharides and inulin decrease resistance of rats to salmonella: protective role of calcium. Gut 53, 530–535.[CrossRef]
    [Google Scholar]
  36. Viswanathan, V. K., Hodges, K. & Hecht, G. ( 2009; ). Enteric infection meets intestinal function: how bacterial pathogens cause diarrhoea. Nat Rev Microbiol 7, 110–119.
    [Google Scholar]
  37. von Ah, U. ( 2006; ). Identification of Bifidobacterium thermophilum RBL67 isolated from baby faeces and partial purification of its bacteriocin. Dissertation no. 16927, ETH Zurich, Zurich, Switzerland.
  38. von Ah, U., Mozzetti, V., Lacroix, C., Kheadr, E. E., Fliss, I. & Meile, L. ( 2007; ). Classification of a moderately oxygen-tolerant isolate from baby faeces as Bifidobacterium thermophilum. BMC Microbiol 7, 79.[CrossRef]
    [Google Scholar]
  39. Wagener, S., Shankar, K. R., Turnock, R. R., Lamont, G. L. & Baillie, C. T. ( 2004; ). Colonic transit time – what is normal? J Pediatr Surg 39, 166–169.[CrossRef]
    [Google Scholar]
  40. Zihler, A., Le Blay, G., de Wouters, T., Lacroix, C., Braegger, C. P., Lehner, A., Tischler, P., Rattei, T., Hächler, H. & Stephan, R. ( 2009; ). In vitro inhibition activity of different bacteriocin-producing Escherichia coli against Salmonella strains isolated from clinical cases. Lett Appl Microbiol 49, 31–38.[CrossRef]
    [Google Scholar]
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