Advertisement

European Journal of Nutrition

, Volume 51, Issue 6, pp 693–705 | Cite as

High-level dietary fibre up-regulates colonic fermentation and relative abundance of saccharolytic bacteria within the human faecal microbiota in vitro

  • Qing Shen
  • Lu Zhao
  • Kieran M. Tuohy
Original Contribution

Abstract

Background

Health authorities around the world advise citizens to increase their intake of foods rich in dietary fibre because of its inverse association with chronic disease. However, a few studies have measured the impact of increasing mixed dietary fibres directly on the composition of the human gut microbiota.

Aims of the study

We studied the impact of high-level mixed dietary fibre intake on the human faecal microbiota using an in vitro three-stage colonic model.

Methods

The colonic model was maintained on three levels of fibre, a basal level of dietary fibre, typical of a Western-style diet, a threefold increased level and back to normal level. Bacterial profiles and short chain fatty acids concentrations were measured.

Results

High-level dietary fibre treatment significantly stimulated the growth of Bifidobacterium, Lactobacillus-Enterococcus group, and Ruminococcus group (p < 0.05) and significantly increased clostridial cluster XIVa and Faecalibacterium prausnitzii in vessel 1 mimicking the proximal colon (p < 0.05). Total short chain fatty acids concentrations increased significantly upon increased fibre fermentation, with acetate and butyrate increasing significantly in vessel 1 only (p < 0.05). Bacterial species richness changed upon increased fibre supplementation. The microbial community and fermentation output returned to initial levels once supplementation with high fibre ceased.

Conclusions

This study shows that high-level mixed dietary fibre intake can up-regulate both colonic fermentation and the relative abundance of saccharolytic bacteria within the human colonic microbiota. Considering the important role of short chain fatty acids in regulating human energy metabolism, this study has implications for the health-promoting potential of foods rich in dietary fibres.

Keywords

Dietary fibre Faecal microbiota Fermentation Short chain fatty acids 

Notes

Acknowledgments

This investigation was supported by the University of Reading, U.K., Reading Overseas Postgraduate Research Studentship scheme, whom the authors would like to thank for their support. The authors declare that they have no conflict of interest.

References

  1. 1.
    Bazzano LA, He J, Ogden LG, Loria CM, Whelton PK (2003) Dietary fiber intake and reduced risk of coronary heart disease in US men and women: the National Health and Nutrition Examination Survey I Epidemiologic Follow-up Study. Arch Intern Med 163:1897–1904CrossRefGoogle Scholar
  2. 2.
    Liu S, Buring JE, Sesso HD, Rimm EB, Willett WC, Manson JE (2002) A prospective study of dietary fiber intake and risk of cardiovascular disease among women. J Am Coll Cardiol 39:49–56CrossRefGoogle Scholar
  3. 3.
    Mozaffarian D, Kumanyika SK, Lemaitre RN, Olson JL, Burke GL, Siscovick DS (2003) Cereal, fruit, and vegetable fiber intake and the risk of cardiovascular disease in elderly individuals. JAMA 289:1659–1666CrossRefGoogle Scholar
  4. 4.
    Bingham SA, Day NE, Luben R, Ferrari P, Slimani N, Norat T, Clavel-Chapelon F, Kesse E, Nieters A, Boeing H, Tjonneland A, Overvad K, Martinez C, Dorronsoro M, Gonzalez CA, Key TJ, Trichopoulou A, Naska A, Vineis P, Tumino R, Krogh V, Bueno-de-Mesquita HB, Peeters PH, Berglund G, Hallmans G, Lund E, Skeie G, Kaaks R, Riboli E (2003) Dietary fibre in food and protection against colorectal cancer in the European Prospective Investigation into Cancer and Nutrition (EPIC): an observational study. Lancet 361:1496–1501CrossRefGoogle Scholar
  5. 5.
    Eaton SB (2006) The ancestral human diet: what was it and should it be a paradigm for contemporary nutrition? Proc Nutr Soc 65:1–6CrossRefGoogle Scholar
  6. 6.
    EFSA Panel on Dietetic Products, Nutrition, and Allergies, European Food Safety Authority (2010) Scientific Opinion on Dietary Reference Values for carbohydrates and dietary fibre. EFSA J 8(3):1462. http://www.efsa.europa.eu/en/efsajournal/pub/1462.htm
  7. 7.
    Dikeman CL, Murphy MR, Fahey GC Jr (2006) Dietary fibers affect viscosity of solutions and simulated human gastric and small intestinal digesta. J Nutr 136:913–919Google Scholar
  8. 8.
    Vuksan V, Jenkins AL, Jenkins DJ, Rogovik AL, Sievenpiper JL, Jovanovski E (2008) Using cereal to increase dietary fiber intake to the recommended level and the effect of fiber on bowel function in healthy persons consuming North American diets. Am J Clin Nutr 88:1256–1262Google Scholar
  9. 9.
    Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101:15718–15723CrossRefGoogle Scholar
  10. 10.
    Bäckhed F, Manchester JK, Semenkovich CF, Gordon JI (2007) Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci USA 104:979–984CrossRefGoogle Scholar
  11. 11.
    Samuel BS, Shaito A, Motoike T, Rey FE, Bäckhed F, Manchester JK, Hammer RE, Williams SC, Crowley J, Yanagisawa M, Gordon JI (2008) Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41. Proc Natl Acad Sci USA 105:16767–16772CrossRefGoogle Scholar
  12. 12.
    Stoddart LA, Smith NJ, Milligan G (2008) International Union of Pharmacology. LXXI. Free fatty acid receptors FFA1, -2, and -3: pharmacology and pathophysiological functions. Pharmacol Rev 60:405–417CrossRefGoogle Scholar
  13. 13.
    Topping DL, Clifton PM (2001) Short-chain fatty acids and human colonic function: roles of resistant starch and nonstarch polysaccharides. Physiol Rev 81:1031–1064Google Scholar
  14. 14.
    Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ (2006) Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 40:235–243CrossRefGoogle Scholar
  15. 15.
    Cani PD, Delzenne NM (2009) The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des 15:1546–1558CrossRefGoogle Scholar
  16. 16.
    Mai V, Draganov PV (2009) Recent advances and remaining gaps in our knowledge of associations between gut microbiota and human health. World J Gastroenterol 15:81–85CrossRefGoogle Scholar
  17. 17.
    Olano-Martin E, Gibson GR, Rastell RA (2002) Comparison of the in vitro bifidogenic properties of pectins and pectic-oligosaccharides. J Appl Microbiol 93:505–511CrossRefGoogle Scholar
  18. 18.
    Rycroft CE, Jones MR, Gibson GR, Rastall RA (2001) A comparative in vitro evaluation of the fermentation properties of prebiotic oligosaccharides. J Appl Microbiol 91:878–887CrossRefGoogle Scholar
  19. 19.
    Gill HS, Rutherfurd KJ, Prasad J, Gopal PK (2000) Enhancement of natural and acquired immunity by Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019). Br J Nutr 83:167–176CrossRefGoogle Scholar
  20. 20.
    Lopez P, Gueimonde M, Margolles A, Suarez A (2010) Distinct Bifidobacterium strains drive different immune responses in vitro. Int J Food Microbiol 138:157–165CrossRefGoogle Scholar
  21. 21.
    Pompei A, Cordisco L, Amaretti A, Zanoni S, Matteuzzi D, Rossi M (2007) Folate production by bifidobacteria as a potential probiotic property. Appl Environ Microbiol 73:179–185CrossRefGoogle Scholar
  22. 22.
    Santos F, Vera JL, van der Heijden R, Valdez G, de Vos WM, Sesma F, Hugenholtz J (2008) The complete coenzyme B12 biosynthesis gene cluster of Lactobacillus reuteri CRL1098. Microbiology 154:81–93CrossRefGoogle Scholar
  23. 23.
    Fooks LJ, Gibson GR (2002) In vitro investigations of the effect of probiotics and prebiotics on selected human intestinal pathogens. FEMS Microbiol Ecol 39:67–75CrossRefGoogle Scholar
  24. 24.
    De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107:14691–14696CrossRefGoogle Scholar
  25. 25.
    Macfarlane GT, Macfarlane S, Gibson GR (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 35:180–187CrossRefGoogle Scholar
  26. 26.
    Martin-Pelaez S, Gibson GR, Martin-Orue SM, Klinder A, Rastall RA, La Ragione RM, Woodward MJ, Costabile A (2008) In vitro fermentation of carbohydrates by porcine faecal inocula and their influence on Salmonella Typhimurium growth in batch culture systems. FEMS Microbiol Ecol 66:608–619CrossRefGoogle Scholar
  27. 27.
    Langendijk PS, Schut F, Jansen GJ, Raangs GC, Kamphuis GR, Wilkinson MH, Welling GW (1995) Quantitative fluorescence in situ hybridization of Bifidobacterium spp. with genus-specific 16S rRNA-targeted probes and its application in fecal samples. Appl Environ Microbiol 61:3069–3075Google Scholar
  28. 28.
    Manz W, Amann R, Ludwig W, Vancanneyt M, Schleifer KH (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum cytophaga-flavobacter-bacteroides in the natural environment. Microbiology 142(Pt 5):1097–1106CrossRefGoogle Scholar
  29. 29.
    Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW (1998) Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 64:3336–3345Google Scholar
  30. 30.
    Harmsen HJM, Eifferich P, Schut F, Welling GW (1999) A16S rRNA-targeted probe for detection of lactobacilli and enterococci in faecal samples by fluorescent in situ hybridization. Microbiol Ecol Health Dis 11:3–12CrossRefGoogle Scholar
  31. 31.
    Harmsen HJ, Wildeboer-Veloo AC, Grijpstra J, Knol J, Degener JE, Welling GW (2000) Development of 16S rRNA-based probes for the Coriobacterium group and the Atopobium cluster and their application for enumeration of Coriobacteriaceae in human feces from volunteers of different age groups. Appl Environ Microbiol 66:4523–4527CrossRefGoogle Scholar
  32. 32.
    Hold GL, Schwiertz A, Aminov RI, Blaut M, Flint HJ (2003) Oligonucleotide probes that detect quantitatively significant groups of butyrate-producing bacteria in human feces. Appl Environ Microbiol 69:4320–4324CrossRefGoogle Scholar
  33. 33.
    Harmsen HJ, Raangs GC, He T, Degener JE, Welling GW (2002) Extensive set of 16S rRNA-based probes for detection of bacteria in human feces. Appl Environ Microbiol 68:2982–2990CrossRefGoogle Scholar
  34. 34.
    Daims H, Bruhl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444CrossRefGoogle Scholar
  35. 35.
    Zhao G, Nyman M, Jonsson JA (2006) Rapid determination of short-chain fatty acids in colonic contents and faeces of humans and rats by acidified water-extraction and direct-injection gas chromatography. Biomed Chromatogr 20:674–682CrossRefGoogle Scholar
  36. 36.
    Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700Google Scholar
  37. 37.
    Sanguinetti CJ, Dias Neto E, Simpson AJ (1994) Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17:914–921Google Scholar
  38. 38.
    Sannasiddappa TH, Costabile A, Gibson GR, Clarke SR (2011) The influence of Staphylococcus aureus on gut microbial ecology in an in vitro continuous culture human colonic model system. PLoS One 6(8):e23227CrossRefGoogle Scholar
  39. 39.
    Tzortzis G, Goulas AK, Gee JM, Gibson GR (2005) A novel galactooligosaccharide mixture increases the bifidobacterial population numbers in a continuous in vitro fermentation system and in the proximal colonic contents of pigs in vivo. J Nutr 135:1726–1731Google Scholar
  40. 40.
    Vulevic J, Drakoularakou A, Yaqoob P, Tzortzis G, Gibson GR (2008) Modulation of the fecal microflora profile and immune function by a novel trans-galactooligosaccharide mixture (B-GOS) in healthy elderly volunteers. Am J Clin Nutr 88:1438–1446Google Scholar
  41. 41.
    Kolida S, Gibson GR (2007) Prebiotic capacity of inulin-type fructans. J Nutr 137:2503S–2506SGoogle Scholar
  42. 42.
    Tuohy KM, Rouzaud GC, Bruck WM, Gibson GR (2005) Modulation of the human gut microflora towards improved health using prebiotics–assessment of efficacy. Curr Pharm Des 11:75–90CrossRefGoogle Scholar
  43. 43.
    Costabile A, Klinder A, Fava F, Napolitano A, Fogliano V, Leonard C, Gibson GR, Tuohy KM (2008) Whole-grain wheat breakfast cereal has a prebiotic effect on the human gut microbiota: a double-blind, placebo-controlled, crossover study. Br J Nutr 99:110–120CrossRefGoogle Scholar
  44. 44.
    Lesmes U, Beards EJ, Gibson GR, Tuohy KM, Shimoni E (2008) Effects of resistant starch type III polymorphs on human colon microbiota and short chain fatty acids in human gut models. J Agric Food Chem 56:5415–5421CrossRefGoogle Scholar
  45. 45.
    van den Broek LA, Hinz SW, Beldman G, Vincken JP, Voragen AG (2008) Bifidobacterium carbohydrases-their role in breakdown and synthesis of (potential) prebiotics. Mol Nutr Food Res 52:146–163CrossRefGoogle Scholar
  46. 46.
    Ataie-Jafari A, Larijani B, Alavi Majd H, Tahbaz F (2009) Cholesterol-lowering effect of probiotic yogurt in comparison with ordinary yogurt in mildly to moderately hypercholesterolemic subjects. Ann Nutr Metab 54:22–27CrossRefGoogle Scholar
  47. 47.
    Le Leu RK, Hu Y, Brown IL, Woodman RJ, Young GP (2010) Synbiotic intervention of Bifidobacterium lactis and resistant starch protects against colorectal cancer development in rats. Carcinogenesis 31:246–251CrossRefGoogle Scholar
  48. 48.
    Worthley DL, Le Leu RK, Whitehall VL, Conlon M, Christophersen C, Belobrajdic D, Mallitt KA, Hu Y, Irahara N, Ogino S, Leggett BA, Young GP (2009) A human, double-blind, placebo-controlled, crossover trial of prebiotic, probiotic, and synbiotic supplementation: effects on luminal, inflammatory, epigenetic, and epithelial biomarkers of colorectal cancer. Am J Clin Nutr 90:578–586CrossRefGoogle Scholar
  49. 49.
    Leitch EC, Walker AW, Duncan SH, Holtrop G, Flint HJ (2007) Selective colonization of insoluble substrates by human faecal bacteria. Environ Microbiol 9:667–679CrossRefGoogle Scholar
  50. 50.
    Walker AW, Ince J, Duncan SH, Webster LM, Holtrop G, Ze X, Brown D, Stares MD, Scott P, Bergerat A, Louis P, McIntosh F, Johnstone AM, Lobley GE, Parkhill J, Flint HJ (2011) Dominant and diet-responsive groups of bacteria within the human colonic microbiota. The ISME J 5:220–230CrossRefGoogle Scholar
  51. 51.
    Belenguer A, Duncan SH, Calder AG, Holtrop G, Louis P, Lobley GE, Flint HJ (2006) Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut. Appl Environ Microbiol 72:3593–3599CrossRefGoogle Scholar
  52. 52.
    Duncan SH, Holtrop G, Lobley GE, Calder AG, Stewart CS, Flint HJ (2004) Contribution of acetate to butyrate formation by human faecal bacteria. Br J Nutr 91:915–923CrossRefGoogle Scholar
  53. 53.
    Louis P, Scott KP, Duncan SH, Flint HJ (2007) Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol 102:1197–1208CrossRefGoogle Scholar
  54. 54.
    Cucchiara S, Iebba V, Conte MP, Schippa S (2009) The microbiota in inflammatory bowel disease in different age groups. Dig Dis 27:252–258CrossRefGoogle Scholar
  55. 55.
    Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, Blugeon S, Bridonneau C, Furet JP, Corthier G, Grangette C, Vasquez N, Pochart P, Trugnan G, Thomas G, Blottiere HM, Dore J, Marteau P, Seksik P, Langella P (2008) Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 105:16731–16736CrossRefGoogle Scholar
  56. 56.
    Sokol H, Seksik P, Furet JP, Firmesse O, Nion-Larmurier I, Beaugerie L, Cosnes J, Corthier G, Marteau P, Dore J (2009) Low counts of Faecalibacterium prausnitzii in colitis microbiota. Inflamm Bowel Dis 15:1183–1189CrossRefGoogle Scholar
  57. 57.
    Walker AW, Duncan SH, McWilliam Leitch EC, Child MW, Flint HJ (2005) 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 71:3692–3700CrossRefGoogle Scholar
  58. 58.
    Probert HM, Apajalahti JH, Rautonen N, Stowell J, Gibson GR (2004) Polydextrose, lactitol, and fructo-oligosaccharide fermentation by colonic bacteria in a three-stage continuous culture system. Appl Environ Microbiol 70:4505–4511CrossRefGoogle Scholar
  59. 59.
    Napolitano A, Costabile A, Martin-Pelaez S, Vitaglione P, Klinder A, Gibson GR, Fogliano V (2009) Potential prebiotic activity of oligosaccharides obtained by enzymatic conversion of durum wheat insoluble dietary fibre into soluble dietary fibre. Nutr Metab Cardiovasc Dis 19:283–290CrossRefGoogle Scholar
  60. 60.
    Arumugam M, Raes J, Pelletier E, Le Paslier D et al. (2011) Enterotypes of the human gut microbiome. Nature 473(7346):174–180Google Scholar
  61. 61.
    Cani PD, Possemiers S, Van de Wiele T, Guiot Y, Everard A, Rottier O, Geurts L, Naslain D, Neyrinck A, Lambert DM, Muccioli GG, Delzenne NM (2009) Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58:1091–1103CrossRefGoogle Scholar
  62. 62.
    Cummings JH, Antoine JM, Azpiroz F, Bourdet-Sicard R, Brandtzaeg P, Calder PC, Gibson GR, Guarner F, Isolauri E, Pannemans D, Shortt C, Tuijtelaars S, Watzl B (2004) PASSCLAIM-gut health and immunity. Eur J Nutr 43(Suppl 2):II118–II173Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of Food and Nutritional Sciences, School of Chemistry, Food and PharmacyThe University of ReadingReadingUK
  2. 2.IASMA Research and Innovation Centre, Fondazione Edmund MachS. Michele all’AdigeItaly

Personalised recommendations