1887

Abstract

Members of the genus are common inhabitants of the proximal gastrointestinal tract of animals such as mice, rats, chickens and pigs, where they form epithelial biofilms. Little is known about the traits that facilitate biofilm formation and gut colonization. This study investigated the ecological role of a glucosyltransferase (GtfA) and inulosucrase (Inu) of TMW1.106 and a fructosyltransferase (FtfA) of LTH5448. experiments using isogenic mutants revealed that GtfA was essential for sucrose-dependent autoaggregation of TMW1.106 cells under acidic conditions, while inactivation of Inu slowed the formation of cell aggregates. Experiments using an biofilm assay showed that GtfA and Inu contributed to biofilm formation of TMW1.106. Experiments using ex-free mice revealed that the ecological performance of the mutant, but not of the or mutant, was reduced in the gastrointestinal tract when in competition with the parental strain. In the absence of competition, the mutant showed delayed colonization of the murine gut relative to the wild-type. In addition, the mutant showed reduced ecological performance in competition experiments with #21. From the evidence provided in this study we conclude that GtfA and Inu confer important ecological attributes of TMW1.106 and contribute to colonization of the mouse gastrointestinal tract.

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2008-01-01
2020-08-07
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References

  1. Banas J. A., Vickerman M. M.. 2003; Glucan-binding proteins of the oral streptococci. Crit Rev Oral Biol Med14:89–99
    [Google Scholar]
  2. Bateup J. M., McConnell M. A., Jenkinson H. F., Tannock G. W.. 1995; Comparison of Lactobacillus strains with respect to bile salt hydrolase activity, colonization of the gastrointestinal tract, and growth rate of the murine host. Appl Environ Microbiol61:1147–1149
    [Google Scholar]
  3. Baumgartner H. K., Montrose M. H.. 2004; Regulated alkali secretion acts in tandem with unstirred layers to regulate mouse gastric surface pH. Gastroenterology126:774–783
    [Google Scholar]
  4. Bello F. D., Walter J., Hertel C., Hammes W. P.. 2001; In vitro study of prebiotic properties of levan-type exopolysaccharides from lactobacilli and non-digestible carbohydrates using denaturing gradient gel electrophoresis. Syst Appl Microbiol24:232–237
    [Google Scholar]
  5. Burne R. A., Chen Y. Y., Wexler D. L., Kuramitsu H., Bowen W. H.. 1996; Cariogenicity of Streptococcus mutans strains with defects in fructan metabolism assessed in a program-fed specific-pathogen-free rat model. J Dent Res75:1572–1577
    [Google Scholar]
  6. Donlan R. M., Costerton J. W.. 2002; Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev15:167–193
    [Google Scholar]
  7. Flint H. J., Duncan S. H., Scott K. P., Lois P.. 2007; Interactions and competition within the microbial community of the human colon: links between diet and health. Environ Microbiol9:1101–1111
    [Google Scholar]
  8. Fuller R., Brooker B. E.. 1974; Lactobacilli which attach to the crop epithelium of the fowl. Am J Clin Nutr27:1305–1312
    [Google Scholar]
  9. Fuller R. P., Barrow P. A., Brooker B. E.. 1978; Bacteria associated with the gastric epithelium of neonatal pigs. Appl Environ Microbiol35:582–591
    [Google Scholar]
  10. Gänzle M. G., Schwab C.. 2005; Exopolysaccharide production by intestinal lactobacilli. In Probiotics and Prebiotics: Scientific Aspects pp83–96 Edited by Tannock G. W.. Wymondham: Horizon Scientific Press;
    [Google Scholar]
  11. Gänzle M. G., Ehmann M., Hammes W. P.. 1998; Modeling of growth of Lactobacillus sanfranciscensis and Candida milleri in response to process parameters of sourdough fermentation. Appl Environ Microbiol64:2616–2623
    [Google Scholar]
  12. Gibbons R. J., Fitzgerald R. J.. 1969; Dextran-induced agglutination of Streptococcus mutans , and its potential role in the formation of microbial dental plaques. J Bacteriol98:341–346
    [Google Scholar]
  13. Gordon H. A., Pesti L.. 1971; The gnotobiotic animal as a tool in the study of host–microbial relationships. Bacteriol Rev35:390–429
    [Google Scholar]
  14. Korakli M., Vogel R. F.. 2006; Structure/function relationship of homopolysaccharide producing glycansucrases and therapeutic potential of their synthesised glycans. Appl Microbiol Biotechnol71:790–803
    [Google Scholar]
  15. Kralj S., van Geel-Schutten G. H., Rahaoui H., Leer R. J., Faber E. J., van der Maarel M. J. E. C., Dijkhuizen L.. 2002; Molecular characterization of a novel glucosyltransferase from Lactobacillus reuteri strain 121 synthesizing a unique, highly branched glucan with α -(1→4) and α -(1→6) glucosidic bonds. Appl Environ Microbiol68:4283–4291
    [Google Scholar]
  16. Kralj S., van Geel-Schutten G. H., Dondorff M. M. G., Kirsanovs S., van der Maarel M. J. E. C., Dijkhuizen L.. 2004; Glucan synthesis in the genus Lactobacillus : isolation and characterization of glucansucrase genes, enzymes and glucan products from six different strains. Microbiology150:3681–3690
    [Google Scholar]
  17. Lundeen S. G., Savage D. C.. 1990; Characterization and purification of bile salt hydrolase from Lactobacillus sp. strain 100-100. J Bacteriol172:4171–4177
    [Google Scholar]
  18. Lynch D. J., Fountain T. L., Mazurkiewicz J. E., Banas J. A.. 2007; Glucan-binding proteins are essential for shaping Streptococcus mutans biofilm architecture. FEMS Microbiol Lett268:158–165
    [Google Scholar]
  19. Munro C., Michalek S. M., Macrina F. L.. 1991; Cariogenicity of Streptococcus mutans V403 glycosyltransferase and fructosyltransferase mutants constructed by allelic exchange. Infect Immun59:2316–2323
    [Google Scholar]
  20. Reuter G.. 2001; The Lactobacillus and Bifidobacterium microflora of the human intestine: composition and succession. Curr Issues Intest Microbiol2:43–53
    [Google Scholar]
  21. Rickard A. H., Gilbert P., High N. J., Kolenbrander P. E., Handley P. S.. 2003; Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol11:94–100
    [Google Scholar]
  22. Rozen R., Steinberg D., Bachrach G.. 2004; Streptococcus mutans fructosyltransferase interactions with glucans. FEMS Microbiol Lett232:39–43
    [Google Scholar]
  23. Russell R. R., Donald A. C., Douglas C. W.. 1983; Fructosyltransferase activity of a glucan-binding protein from Streptococcus mutans . J Gen Microbiol129:3243–3250
    [Google Scholar]
  24. Savage D. C., Dubos R., Schaedler R. W.. 1968; The gastrointestinal epithelium and its autochthonous bacterial flora. J Exp Med127:67–76
    [Google Scholar]
  25. Schwab C., Gänzle M. G.. 2006; Effect of membrane lateral pressure on the expression of fructosyltransferases in Lactobacillus reuteri . Syst Appl Microbiol29:89–99
    [Google Scholar]
  26. Schwab C., Walter J., Tannock G. W., Vogel R. F., Gänzle M. G.. 2007; Sucrose utilization and impact of sucrose on glycosyltransferase expression in Lactobacillus reuteri . Syst Appl Microbiol30:433–443
    [Google Scholar]
  27. Tannock G. W.. 1992; Lactic microflora of pigs, mice and rats. In The Lactic Acid Bacteria , vol. 1. The Lactic Acid Bacteria in Health and Disease pp21–48 Edited by Wood B. J. B.. London, UK: Elsevier Applied Science;
    [Google Scholar]
  28. Tannock G. W.. 1997; Normal microbiota of the gastrointestinal tract of rodents. In Gastrointestinal Microbiology vol II pp187–215 Edited by Mackie R. I.. White B. A., Isaacson R. E.. London, UK: Chapman and Hall;
    [Google Scholar]
  29. Tannock G. W., Crichton C., Welling G. W., Koopman J. P., Midtvedt T.. 1988; Reconstitution of the gastrointestinal microflora of lactobacillus-free mice. Appl Environ Microbiol54:2971–2975
    [Google Scholar]
  30. Tannock G. W., Ghazally S., Walter J., Loach D., Cook G., Surette M., Simmers C., Bremer P., Dal Bello F., Hertel C.. 2005; Ecological behavior of Lactobacillus reuteri is affected by mutation of the luxS gene. Appl Environ Microbiol71:8419–8425
    [Google Scholar]
  31. Tieking M., Korakli M., Ehrmann M. A., Gänzle M. G., Vogel R. F.. 2003; In situ production of exopolysaccharides during sourdough fermentation by cereal and intestinal isolates of lactic acid bacteria. Appl Environ Microbiol69:945–952
    [Google Scholar]
  32. Tieking M., Kaditzky S., Valcheva R., Korakli M., Vogel R. F., Gänzle M. G.. 2005; Extracellular homopolysaccharides and oligosaccharides from intestinal lactobacilli. J Appl Microbiol99:692–702
    [Google Scholar]
  33. van Hijum S. A. F. T., van Geel-Schutten G. H., Rahaoui H., van der Maarel M. J. E. C., Dijkhuizen L.. 2002; Characterization of a novel fructosyltransferase from Lactobacillus reuteri that synthesizes high-molecular-weight inulin and inulin oligosaccharides. Appl Environ Microbiol68:4390–4398
    [Google Scholar]
  34. van Hijum S. A. F. T., Kralj S., Ozimek L. K., Dijkhuizen L., van Geel-Schutten G. H.. 2006; Structure–function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiol Mol Biol Rev70:157–176
    [Google Scholar]
  35. Walter J.. 2005; The microecology of lactobacilli in the gastrointestinal tract. In Probiotics and Prebiotics: Scientific Aspects pp51–82 Edited by Tannock G. W. Wymondham: Horizon Scientific Press;
    [Google Scholar]
  36. Walter J., Heng N. C. K., Hammes W. P., Loach D. M., Tannock G. W., Hertel C.. 2003; Identification of Lactobacillus reuteri genes specifically induced in the mouse gastrointestinal tract. Appl Environ Microbiol69:2044–2051
    [Google Scholar]
  37. Walter J., Chagnaud P., Tannock G. W., Loach D. M., Dal Bello F., Jenkinson H. F., Hammes W. P., Hertel C.. 2005; A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MrsB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl Environ Microbiol71:979–986
    [Google Scholar]
  38. Walter J., Loach D. M., Alqumber M., Rockel C., Hermann C., Pfitzenmaier M., Tannock G. W.. 2007; d-Alanyl ester depletion of teichoic acids in Lactobacillus reuteri 100-23 results in impaired colonization of the mouse gastrointestinal tract. Environ Microbiol9:1750–1760
    [Google Scholar]
  39. Wesney E., Tannock G. W.. 1979; Association of rat, pig and fowl biotypes of lactobacilli with the stomach of gnotobiotic mice. Microb Ecol5:35–42
    [Google Scholar]
  40. Yamashita Y., Bowen W. H., Burne R. A., Kuramitsu H. K.. 1993; Role of Streptococcus mutans gtf genes in caries induction in the specific-pathogen-free rat model. Infect Immun61:3811–3817
    [Google Scholar]
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