Home LiteratureArticle Details
PMID: 18539803 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Exopolysaccharides produced by intestinal Bifidobacterium strains act as fermentable substrates for human intestinal bacteria.

Applied and environmental microbiology ·Vol. 74 ·No. 15 ·2008-08-00 ·Pages 4737-45

Salazar N, Gueimonde M, Hernández-Barranco AM, Ruas-Madiedo P, de los Reyes-Gavilán CG

Abstract

Eleven exopolysaccharides (EPS) isolated from different human intestinal Bifidobacterium strains were tested in fecal slurry batch cultures and compared with glucose and the prebiotic inulin for their abilities to act as fermentable substrates for intestinal bacteria. During incubation, the increases in levels of short-chain fatty acids (SCFA) were considerably more pronounced in cultures with EPS, glucose, and inulin than in controls without carbohydrates added, indicating that the substrates assayed were fermented by intestinal bacteria. Shifts in molar proportions of SCFA during incubation with EPS and inulin caused a decrease in the acetic acid-to-propionic acid ratio, a possible indicator of the hypolipidemic effect of prebiotics, with the lowest values for this parameter being obtained for EPS from the species Bifidobacterium longum and from Bifidobacterium pseudocatenulatum strain C52. This behavior was contrary to that found with glucose, a carbohydrate not considered to be a prebiotic and for which a clear increase of this ratio was obtained during incubation. Quantitative real-time PCR showed that EPS exerted a moderate bifidogenic effect, which was comparable to that of inulin for some polymers but which was lower than that found for glucose. PCR-denaturing gradient gel electrophoresis of 16S rRNA gene fragments using universal primers was employed to analyze microbial groups other than bifidobacteria. Changes in banding patterns during incubation with EPS indicated microbial rearrangements of Bacteroides and Escherichia coli relatives. Moreover, the use of EPS from B. pseudocatenulatum in fecal cultures from some individuals accounted for the prevalence of Desulfovibrio and Faecalibacterium prausnitzii, whereas incubation with EPS from B. longum supported populations close to Anaerostipes, Prevotella, and/or Oscillospira. Thus, EPS synthesized by intestinal bifidobacteria could act as fermentable substrates for microorganisms in the human gut environment, modifying interactions among intestinal populations.

MeSH Terms
Bifidobacterium/genetics,isolation & purification,metabolism DNA, Bacterial/genetics Fermentation Humans Intestines/microbiology Polymerase Chain Reaction Polysaccharides, Bacterial/biosynthesis,metabolism RNA, Bacterial/genetics RNA, Ribosomal, 16S/genetics Substrate Specificity
Chemicals
DNA, Bacterial Polysaccharides, Bacterial RNA, Bacterial RNA, Ribosomal, 16S
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Salazar Nuria
Departamento de Microbiología y Bioquímica de Productos Lácteos, Instituto de Productos Lácteos de Asturias, Carretera de Infiesto s/n (P.O. Box 85), 33300 Villaviciosa, Asturias, Spain.
Gueimonde Miguel
Hernández-Barranco Ana María
Ruas-Madiedo Patricia
de los Reyes-Gavilán Clara G
References (43)
43 references, click to expand
  1. Biodiversity of exopolysaccharides produced by Streptococcus thermophilus strains is reflected in their production and their molecular and functional characteristics.
    Appl Environ Microbiol. 2004 Feb;70(2):900-12 PMID: 14766570
  2. Interindividual differences in microbial counts and biochemical-associated variables in the feces of healthy Spanish adults.
    Dig Dis Sci. 2006 Apr;51(4):737-43 PMID: 16614997
  3. Metabolism by bifidobacteria and lactic acid bacteria of polysaccharides from wheat and rye, and exopolysaccharides produced by Lactobacillus sanfranciscensis.
    J Appl Microbiol. 2002;92(5):958-65 PMID: 11972702
  4. In vitro fermentability of dextran, oligodextran and maltodextrin by human gut bacteria.
    Br J Nutr. 2000 Mar;83(3):247-55 PMID: 10884713
  5. Energy sources of major intestinal fermentative anaerobes.
    Am J Clin Nutr. 1979 Jan;32(1):158-63 PMID: 367143
  6. Lactate is mainly fermented to butyrate by human intestinal microfloras but inter-individual variation is evident.
    J Appl Microbiol. 2005;99(1):201-12 PMID: 15960680
  7. Ecology of uncultivated Oscillospira species in the rumen of cattle, sheep, and reindeer as assessed by microscopy and molecular approaches.
    Appl Environ Microbiol. 2003 Nov;69(11):6808-15 PMID: 14602644
  8. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics.
    J Nutr. 1995 Jun;125(6):1401-12 PMID: 7782892
  9. Growth requirements and fermentation products of Fusobacterium prausnitzii, and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov.
    Int J Syst Evol Microbiol. 2002 Nov;52(Pt 6):2141-2146 PMID: 12508881
  10. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA.
    Appl Environ Microbiol. 1993 Mar;59(3):695-700 PMID: 7683183
  11. Comparison of maintenance energy expenditures and growth yields among several rumen bacteria grown on continuous culture.
    Appl Environ Microbiol. 1979 Mar;37(3):537-43 PMID: 16345359
  12. New real-time quantitative PCR procedure for quantification of bifidobacteria in human fecal samples.
    Appl Environ Microbiol. 2004 Jul;70(7):4165-9 PMID: 15240297
  13. Growth of a human intestinal Desulfovibrio desulfuricans in continuous cultures containing defined populations of saccharolytic and amino acid fermenting bacteria.
    J Appl Microbiol. 1998 Aug;85(2):372-80 PMID: 9750310
  14. Oligofructose and long-chain inulin: influence on the gut microbial ecology of rats associated with a human faecal flora.
    Br J Nutr. 2001 Aug;86(2):291-300 PMID: 11502244
  15. A two-stage continuous culture system to study the effect of supplemental alpha-lactalbumin and glycomacropeptide on mixed cultures of human gut bacteria challenged with enteropathogenic Escherichia coli and Salmonella serotype Typhimurium.
    J Appl Microbiol. 2003;95(1):44-53 PMID: 12807453
  16. Prebiotic effects of chicory inulin in the simulator of the human intestinal microbial ecosystem.
    FEMS Microbiol Ecol. 2004 Dec 27;51(1):143-53 PMID: 16329863
  17. pH and peptide supply can radically alter bacterial populations and short-chain fatty acid ratios within microbial communities from the human colon.
    Appl Environ Microbiol. 2005 Jul;71(7):3692-700 PMID: 16000778
  18. Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut.
    Appl Environ Microbiol. 1999 Nov;65(11):4799-807 PMID: 10543789
  19. Prevotella copri sp. nov. and Prevotella stercorea sp. nov., isolated from human faeces.
    Int J Syst Evol Microbiol. 2007 May;57(Pt 5):941-946 PMID: 17473237
  20. How host-microbial interactions shape the nutrient environment of the mammalian intestine.
    Annu Rev Nutr. 2002;22:283-307 PMID: 12055347
  21. Fermentation in the human large intestine and the available substrates.
    Am J Clin Nutr. 1987 May;45(5 Suppl):1243-55 PMID: 3034048
  22. Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides.
    Physiol Rev. 2001 Jul;81(3):1031-64 PMID: 11427691
  23. Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose.
    Appl Environ Microbiol. 2006 Dec;72(12):7835-41 PMID: 17056678
  24. Anaerostipes caccae gen. nov., sp. nov., a new saccharolytic, acetate-utilising, butyrate-producing bacterium from human faeces.
    Syst Appl Microbiol. 2002 Apr;25(1):46-51 PMID: 12086188
  25. Vitamin B12-dependent propionate production by the ruminal bacterium Prevotella ruminicola 23.
    Appl Environ Microbiol. 1992 Jul;58(7):2331-3 PMID: 1637169
  26. In vitro fermentation of sugar beet arabinan and arabino-oligosaccharides by the human gut microflora.
    J Appl Microbiol. 2006 Feb;100(2):407-14 PMID: 16430518
  27. Effects of fructans-type prebiotics on lipid metabolism.
    Am J Clin Nutr. 2001 Feb;73(2 Suppl):456S-458S PMID: 11157357
  28. Culture-dependent and culture-independent qualitative analysis of probiotic products claimed to contain bifidobacteria.
    Int J Food Microbiol. 2005 Jul 15;102(2):221-30 PMID: 15992621
  29. Exopolysaccharides produced by probiotic strains modify the adhesion of probiotics and enteropathogens to human intestinal mucus.
    J Food Prot. 2006 Aug;69(8):2011-5 PMID: 16924934
  30. Comparison of bacterial diversity along the human intestinal tract by direct cloning and sequencing of 16S rRNA genes.
    FEMS Microbiol Ecol. 2005 Oct 1;54(2):219-31 PMID: 16332321
  31. Screening of exopolysaccharide-producing Lactobacillus and Bifidobacterium strains isolated from the human intestinal microbiota.
    Appl Environ Microbiol. 2007 Jul;73(13):4385-8 PMID: 17483284
  32. Molecular analysis of fecal microbiota in elderly individuals using 16S rDNA library and T-RFLP.
    Microbiol Immunol. 2003;47(8):557-70 PMID: 14524616
  33. In vitro study of prebiotic properties of levan-type exopolysaccharides from Lactobacilli and non-digestible carbohydrates using denaturing gradient gel electrophoresis.
    Syst Appl Microbiol. 2001 Jul;24(2):232-7 PMID: 11518326
  34. Effects of alternative dietary substrates on competition between human colonic bacteria in an anaerobic fermentor system.
    Appl Environ Microbiol. 2003 Feb;69(2):1136-42 PMID: 12571040
  35. Lactate-utilizing bacteria, isolated from human feces, that produce butyrate as a major fermentation product.
    Appl Environ Microbiol. 2004 Oct;70(10):5810-7 PMID: 15466518
  36. Variations in concentrations of bacterial metabolites, enzyme activities, moisture, pH and bacterial composition between and within individuals in faeces of seven healthy adults.
    J Appl Bacteriol. 1994 Aug;77(2):185-94 PMID: 7961190
  37. Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut.
    Appl Environ Microbiol. 2006 May;72(5):3593-9 PMID: 16672507
  38. Effects of inulin on faecal bifidobacteria in human subjects.
    Br J Nutr. 1999 Nov;82(5):375-82 PMID: 10673910
  39. Bifidobacterial diversity determined by culturing and by 16S rDNA sequence analysis in feces and mucosa from ten healthy Spanish adults.
    Dig Dis Sci. 2006 Oct;51(10):1878-85 PMID: 16967311
  40. Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin.
    Gastroenterology. 1995 Apr;108(4):975-82 PMID: 7698613
  41. Effects of the in vitro fermentation of oligofructose and inulin by bacteria growing in the human large intestine.
    J Appl Bacteriol. 1993 Oct;75(4):373-80 PMID: 8226394
  42. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis.
    Nat Rev Microbiol. 2008 Feb;6(2):121-31 PMID: 18180751
  43. Nondigestible oligosaccharides enhance bacterial colonization resistance against Clostridium difficile in vitro.
    Appl Environ Microbiol. 2003 Apr;69(4):1920-7 PMID: 12676665
Article Info
Journal
Applied and environmental microbiology
Abbr.
Appl Environ Microbiol
ISSN
1098-5336
Published
2008-08-00
Epub
2008-00-06
Pages
4737-45
Language
English
Region
United States
NLM ID
7605801
PMCID
PMC2519331
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]