Skip to main content
×
×
Home

Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii

  • Carlett Ramirez-Farias (a1), Kathleen Slezak (a1), Zoë Fuller (a2), Alan Duncan (a2), Grietje Holtrop (a3) and Petra Louis (a1)...
Abstract

Prebiotics are food ingredients that improve health by modulating the colonic microbiota. The bifidogenic effect of the prebiotic inulin is well established; however, it remains unclear which species of Bifidobacterium are stimulated in vivo and whether bacterial groups other than lactic acid bacteria are affected by inulin consumption. Changes in the faecal microbiota composition were examined by real-time PCR in twelve human volunteers after ingestion of inulin (10 g/d) for a 16-d period in comparison with a control period without any supplement intake. The prevalence of most bacterial groups examined did not change after inulin intake, although the low G+C % Gram-positive species Faecalibacterium prausnitzii exhibited a significant increase (10·3 % for control period v. 14·5 % during inulin intake, P = 0·019). The composition of the genus Bifidobacterium was studied in four of the volunteers by clone library analysis. Between three and five Bifidobacterium spp. were found in each volunteer. Bifidobacterium adolescentis and Bifidobacterium longum were present in all volunteers, and Bifidobacterium pseudocatenulatum, Bifidobacterium animalis, Bifidobacterium bifidum and Bifidobacterium dentium were also detected. Real-time PCR was employed to quantify the four most prevalent Bifidobacterium spp., B. adolescentis, B. longum, B. pseudocatenulatum and B. bifidum, in ten volunteers carrying detectable levels of bifidobacteria. B. adolescentis showed the strongest response to inulin consumption, increasing from 0·89 to 3·9 % of the total microbiota (P = 0·001). B. bifidum was increased from 0·22 to 0·63 % (P < 0·001) for the five volunteers for whom this species was present.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii
      Available formats
      ×
Copyright
Corresponding author
*Corresponding author: Petra Louis, fax +44 1224 716687, email p.louis@rowett.ac.uk
References
Hide All
1Flint, HJ, Louis, P, Scott, KP & Duncan, SH (2007) Commensal bacteria in health and disease. In Virulence Mechanisms of Bacterial Pathogens, pp. 101114 [Brogden, KA, editor]. Washington, DC: ASM Press.
2Gibson, GR, Probert, HM, Van Loo, J, Rastall, RA & Roberfroid, MB (2004) Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutr Res Rev 17, 259275.
3Macfarlane, S, Macfarlane, GT & Cummings, JH (2006) Review article: prebiotics in the gastrointestinal tract. Aliment Pharmacol Ther 24, 701714.
4Guarner, F (2005) Inulin and oligofructose: impact on intestinal diseases and disorders. Br J Nutr 93, S61S65.
5Matsuki, T, Watanabe, K, Tanaka, R, Fukuda, M & Oyaizu, H (1999) Distribution of bifidobacterial species in human intestinal microflora examined with 16S rRNA-gene-targeted species-specific primers. Appl Environ Microbiol 65, 45064512.
6Satokari, RM, Vaughan, EE, Akkermans, AD, Saarela, M & de Vos, WM (2001) Bifidobacterial species diversity in human feces detected by genus-specific PCR and denaturing gradient gel electrophoresis. Appl Environ Microbiol 67, 504513.
7Mullié, C, Odou, MF, Singer, E, Romond, MB & Izard, D (2003) Multiplex PCR using 16S rRNA gene-targeted primers for the identification of bifidobacteria from human origin. FEMS Microbiol Lett 222, 129136.
8Mangin, I, Suau, A, Magne, F, Garrido, D, Gotteland, M, Neut, C & Pochart, P (2006) Characterization of human intestinal bifidobacteria using competitive PCR and PCR-TTGE. FEMS Microbiol Ecol 55, 2837.
9Rossi, M, Corradini, C, Amaretti, A, Nicolini, M, Pompei, A, Zanoni, S & Matteuzzi, D (2005) Fermentation of fructooligosaccharides and inulin by bifidobacteria: a comparative study of pure and fecal cultures. Appl Environ Microbiol 71, 61506158.
10Food Quality and Standards Service & Food and Agriculture Organization of the United Nations (FAO) (2007) FAO Technical Meeting on prebiotics, September 15–16.
11Duncan, SH, Hold, GL, Harmsen, HJM, Stewart, CS & Flint, HJ (2002) 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 52, 21412146.
12Duncan, SH, Aminov, RI, Scott, KP, Louis, P, Stanton, TB & Flint, HJ (2006) Proposal of Roseburia faecis sp. nov. Roseburia hominis sp. nov. and Roseburia inulinivorans sp. nov., based on isolates from human faeces. Int J Syst Evol Microbiol 56, 24372441.
13Belenguer, 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, 35933599.
14Falony, G, Vlachou, A, Verbrugghe, K & De Vuyst, L (2006) Cross-feeding between Bifidobacterium longum BB536 and acetate-converting, butyrate-producing colon bacteria during growth on oligofructose. Appl Environ Microbiol 72, 78357841.
15Bourriaud, C, Robins, RJ, Martin, L, Kozlowski, F, Tenailleau, E, Cherbut, C & Michel, C (2005) Lactate is mainly fermented to butyrate by human intestinal microfloras but inter-individual variation is evident. J Appl Microbiol 99, 201212.
16Walker, 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, 36923700.
17Belenguer, A, Duncan, SH, Holtrop, G, Anderson, SE, Lobley, GE & Flint, HJ (2007) Impact of pH on lactate formation and utilization by human fecal microbial communities. Appl Environ Microbiol 73, 65266533.
18Zoetendal, EG, Collier, CT, Koike, S, Mackie, RI & Gaskins, HR (2004) Molecular ecological analysis of the gastrointestinal microbiota: a review. J Nutr 134, 465472.
19Fuller, Z, Louis, P, Mihajlovski, A, Rungapamestry, V, Ratcliffe, B & Duncan, AJ (2007) Influence of cabbage processing methods and prebiotic manipulation of colonic microflora on glucosinolate breakdown in man. Br J Nutr 98, 364372.
20Gueimonde, M, Tölkkö, S, Korpimäki, T & Salminen, S (2004) New real-time quantitative PCR procedure for quantification of bifidobacteria in human fecal samples. Appl Environ Microbiol 70, 41654169.
21Richardson, AJ, Calder, GC, Stewart, CS & Smith, A (1989) Simultaneous determination of volatile and non-volatile fermentation products of anaerobes by capillary gas chromatography. Lett Appl Microbiol 9, 58.
22Cole, JR, Chai, B, Farris, RJ, Wang, Q, Kulam-Syed-Mohideen, AS, McGarrell, DM, Bandela, AM, Cardenas, E, Garrity, GM & Tiedje, JM (2007) The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35, D169D172.
23Aminov, RI, Walker, AW, Duncan, SH, Harmsen, HJ, Welling, GW & Flint, HJ (2006) Molecular diversity, cultivation, and improved detection by fluorescent in situ hybridisation of a dominant group of human gut bacteria related to Roseburia spp. or Eubacterium rectale. Appl Environ Microbiol 72, 63716376.
24Louis, P & Flint, HJ (2007) Development of a semiquantitative degenerate real-time PCR-based assay for estimation of numbers of butyryl-coenzyme A (CoA) CoA transferase genes in complex bacterial samples. Appl Environ Microbiol 73, 20092012.
25Flint, HJ, McPherson, CA & Bisset, J (1989) Molecular cloning of genes from Ruminococcus flavefaciens encoding xylanase and beta(1-3,1-4)glucanase activities. Appl Environ Microbiol 55, 12301233.
26Bookout, AL, Cummins, CL, Kramer, MF, Pesola, JM & Mangelsdorf, DJ (2006) High-throughput real-time quantitative reverse transcription PCR. In Current Protocols in Molecular Biology, pp. 1581528 [Ausubel, FM, Brent, R, Kingston, RE, Moore, DD, Seidman, JG, Smith, JA and Struhl, K, editors]. Hoboken, NJ: John Wiley & Sons, Inc.
27Bartosch, S, Fite, A, Macfarlane, GT & McMurdo, ME (2004) Characterization of bacterial communities in feces from healthy elderly volunteers and hositalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol 70, 35753581.
28Matsuki, T, Watanabe, K, Fujimoto, J, Miyamoto, Y, Takada, T, Matsumoto, K, Oyaizu, H & Tanaka, R (2002) Development of 16S rRNA-gene-targeted group-specific primers for the detection and identification of predominant bacteria in human feces. Appl Environ Microbiol 68, 54455451.
29Ewing, B & Green, P (1998) Basecalling of automated sequencer traces using Phred. II. Error probabilities. Genome Res 8, 186194.
30Ewing, B, Hillier, L, Wendl, M & Green, P (1998) Basecalling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Res 8, 175185.
31Chou, HH & Holmes, MH (2001) DNA sequence quality trimming and vector removal. Bioinformatics 17, 10931104.
32Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 17921797.
33Chenna, R, Sugawara, H, Koike, T, Lopez, R, Gibson, TJ, Higgins, DG & Thompson, JD (2003) Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res 31, 34973500.
34Clamp, M, Cuff, J, Searle, SM & Barton, GJ (2004) The Jalview Java alignment editor. Bioinformatics 20, 426427.
35Felsenstein, J (2005) PHYLIP (PhylogenyInference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, http://evolution.genetics.washington.edu/phylip.html.
36Schloss, PD & Handelsman, J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71, 15011506.
37Altschul, SF, Gish, W, Miller, W, Myers, EW & Lipman, DJ (1990) Basic local alignment search tool. J Mol Biol 215, 403410.
38Collins, MD, Lawson, PA, Willems, A, Cordoba, JJ, Fernandez-Garayzabal, J, Garcia, P, Cai, J, Hippe, H & Farrow, JA (1994) The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44, 812826.
39Kleessen, B, Schwarz, S, Boehm, A, Fuhrmann, H, Richter, A, Henle, T & Krueger, M (2007) Jerusalem artichoke and chicory inulin in bakery products affect faecal microbiota of healthy volunteers. Br J Nutr 98, 540549.
40Nyman, M (2002) Fermentation and bulking capacity of indigestible carbohydrates: the case of inulin and oligofructose. Br J Nutr 87, S163S168.
41Duncan, SH, Belenguer, A, Holtrop, G, Johnstone, AM, Flint, HJ & Lobley, GE (2007) Reduced dietary intake of carbohydrates by obese subjects results in dereased concentrations of butyrate and butyrate-producing bacteria in feces. Appl Environ Microbiol 73, 10731078.
42Duncan, SH, Hold, GL, Barcenilla, A, Stewart, CS & Flint, HJ (2002) Roseburia intestinalis sp. nov. a novel saccharolytic, butyrate-producing bacterium from human faeces. Int J Syst Evol Microbiol 52, 16151620.
43Harmsen, HJM, Raangs, GC, Franks, AH, Wildeboer-Veloo, ACM & Welling, GW (2002) The effect of the prebiotic inulin and the probiotic Bifidobacterium longum on the fecal microflora of healthy volunteers measured by FISH and DGGE. Microbial Ecol Health Dis 14, 211219.
44Masco, L, Huys, G, De Brandt, E, Temmerman, R & Swings, J (2005) Culture-dependent and culture-independent qualitative analysis of probiotic products claimed to contain bifidobacteria. Int J Food Microbiol 102, 221230.
45Ouwehand, AC, Bergsma, N, Parhiala, R, Lahtinen, S, Gueimonde, M, Finne-Soveri, H, Strandberg, T, Pitkäla, K & Salminen, S (2008) Bifidobacterium microbiota and parameters of immune function in elderly subjects. FEMS Immunol Med Microbiol 53, 1825.
46Liu, C, Song, Y, McTeague, M, Vu, AW, Wexler, H & Finegold, SM (2003) Rapid identification of the species of the Bacteroides fragilis group by multiplex PCR assays using group- and species-specific primers. FEMS Microbiol Lett 222, 916.
47Rinttilä, T, Kassinen, A, Malinen, E, Krogius, L & Palva, A (2004) Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 97, 11661177.
48Hold, 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, 43204324.
49Lay, C, Sutren, M, Rochet, V, Saunier, K, Doré, J & Rigottier-Gois, L (2005) Design and validation of 16S rRNA probes to enumerate members of the Clostridium leptum subgroup in human faecal microbiota. Environ Microbiol 7, 933946.
50Sghir, A, Gramet, G, Suau, A, Rochet, V, Pochart, P & Doré, J (2000) Quantification of bacterial groups within human fecal flora by oligonucleotide probe hybridization. Appl Environ Microbiol 66, 22632266.
51Wang, RF, Cao, WW & Cerniglia, CE (1996) PCR detection and quantification of predominant anaerobic bacteria in human and animal fecal samples. Appl Environ Microbiol 62, 12421247.
52Suau, A, Rochet, V, Sghir, A, Gramet, G, Brewaeys, S, Sutren, M, Rigottier-Gois, L & Doré, J (2001) Fusobacterium prausnitzii and related species represent a dominant group within the human fecal flora. Syst Appl Microbiol 24, 139145.
53Harmsen, 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, 29822990.
54Malinen, E, Rinttilä, T, Kajander, K, Mättö, J, Kassinen, A, Krogius, L, Saarela, M, Korpela, R & Palva, A (2005) Analysis of the fecal microbiota of irritable bowel syndrome patients and healthy controls with real-time PCR. Am J Gastroenterol 100, 373382.
55Barcenilla, A, Pryde, SE, Martin, JC, Duncan, SH, Stewart, CS, Henderson, C & Flint, HJ (2000) Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 66, 16541661.
56Louis, P, Duncan, SH, McCrae, SI, Millar, J, Jackson, MS & Flint, HJ (2004) Restricted distribution of the butyrate kinase pathway among butyrate-producing bacteria from the human colon. J Bacteriol 186, 20992106.
57Barcenilla, A (1999) Diversity of the butyrate-producing microflora of the human gut. PhD Thesis. Robert Gordon University, Aberdeen, UK..
58Dabek, M, McCrae, SI, Stevens, VJ, Duncan, SH & Louis, P (2008) Distribution of β-glucosidase and β-glucuronidase activity and of β-glucuronidase gene gus in human colonic bacteria. FEMS Microbiol Ecol (Epublication ahead of print version 4 June 2008).
59Varel, VH & Dehority, BA (1989) Cellulolytic bacteria and protozoa from bison, cattle-bison hybrids, and cattle fed three alfalfa-corn diets. Appl Environ Microbiol 55, 148153.
60Whitehead, TR & Hespell, RB (1990) The genes for three xylan-degrading activities from Bacteroides ovatus are clustered in a 3·8-kilobase region. J Bacteriol 172, 24082412.
61Cato, EP & Johnson, JL (1976) Reinstatement of species rank for Bacteroides fragilis, B. ovatus, B. distasonis, B. thetaiotaomicron, and B. vulgatus: designation of neotype strains for Bacteroides fragilis (Veillon and Zuber) Castellani and Chalmers and Bacteroides thetaiotaomicron (Distaso) Castellani and Chalmers. Int J Syst Bacteriol 26, 230237.
62Reuter, G (1963) Vergleichende Untersuchungen über die Bifidus-Flora des Säuglings- und Erwachsenenstuhl. Zentralbl Bakteriol Parasitenkd Orig Abt I 191, 486507.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed