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      Review article: dietary fibre–microbiota interactions

      review-article
      1 , 1 ,
      Alimentary Pharmacology & Therapeutics
      John Wiley and Sons Inc.

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          Summary

          Background

          Application of modern rapid DNA sequencing technology has transformed our understanding of the gut microbiota. Diet, in particular plant‐based fibre, appears critical in influencing the composition and metabolic activity of the microbiome, determining levels of short‐chain fatty acids ( SCFAs) important for intestinal health.

          Aim

          To assess current epidemiological, experimental and clinical evidence of how long‐term and short‐term alterations in dietary fibre intake impact on the microbiome and metabolome.

          Methods

          A Medline search including items ‘intestinal microbiota’, ‘nutrition’, ‘diet’, ‘dietary fibre’, ‘ SCFAs’ and ‘prebiotic effect’ was performed.

          Results

          Studies found evidence of fibre‐influenced differences in the microbiome and metabolome as a consequence of habitual diet, and of long‐term or short‐term intervention (in both animals and humans).

          Conclusions

          Agrarian diets high in fruit/legume fibre are associated with greater microbial diversity and a predominance of Prevotella over Bacteroides. ‘Western’‐style diets, high in fat/sugar, low in fibre, decrease beneficial Firmicutes that metabolise dietary plant‐derived polysaccharides to SCFAs and increase mucosa‐associated Proteobacteria (including enteric pathogens). Short‐term diets can also have major effects, particularly those exclusively animal‐based, and those high‐protein, low‐fermentable carbohydrate/fibre ‘weight‐loss’ diets, increasing the abundance of Bacteroides and lowering Firmicutes, with long‐term adherence to such diets likely increasing risk of colonic disease. Interventions to prevent intestinal inflammation may be achieved with fermentable prebiotic fibres that enhance beneficial Bifidobacteria or with soluble fibres that block bacterial–epithelial adherence (contrabiotics). These mechanisms may explain many of the differences in microbiota associated with long‐term ingestion of a diet rich in fruit and vegetable fibre.

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          Most cited references71

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          Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces.

          Weight loss diets for humans that are based on a high intake of protein but low intake of fermentable carbohydrate may alter microbial activity and bacterial populations in the large intestine and thus impact on gut health. In this study, 19 healthy, obese (body mass index range, 30 to 42) volunteers were given in succession three different diets: maintenance (M) for 3 days (399 g carbohydrate/day) and then high protein/medium (164 g/day) carbohydrate (HPMC) and high protein/low (24 g/day) carbohydrate (HPLC) each for 4 weeks. Stool samples were collected at the end of each dietary regimen. Total fecal short-chain fatty acids were 114 mM, 74 mM, and 56 mM (P < 0.001) for M, HPMC, and HPLC diets, respectively, and there was a disproportionate reduction in fecal butyrate (18 mM, 9 mM, and 4 mM, respectively; P < 0.001) with decreasing carbohydrate. Major groups of fecal bacteria were monitored using nine 16S rRNA-targeted fluorescence in situ hybridization probes, relative to counts obtained with the broad probe Eub338. No significant change was seen in the relative counts of the bacteroides (Bac303) (mean, 29.6%) or the clostridial cluster XIVa (Erec482, 23.3%), cluster IX (Prop853, 9.3%), or cluster IV (Fprau645, 11.6%; Rbro730 plus Rfla729, 9.3%) groups. In contrast, the Roseburia spp. and Eubacterium rectale subgroup of cluster XIVa (11%, 8%, and 3% for M, HPMC, and HPLC, respectively; P < 0.001) and bifidobacteria (4%, 2.1%, and 1.9%, respectively; P = 0.026) decreased as carbohydrate intake decreased. The abundance of butyrate-producing bacteria related to Roseburia spp. and E. rectale correlated well with the decline in fecal butyrate.
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            Towards the human intestinal microbiota phylogenetic core.

            The paradox of a host specificity of the human faecal microbiota otherwise acknowledged as characterized by global functionalities conserved between humans led us to explore the existence of a phylogenetic core. We investigated the presence of a set of bacterial molecular species that would be altogether dominant and prevalent within the faecal microbiota of healthy humans. A total of 10 456 non-chimeric bacterial 16S rRNA sequences were obtained after cloning of PCR-amplified rDNA from 17 human faecal DNA samples. Using alignment or tetranucleotide frequency-based methods, 3180 operational taxonomic units (OTUs) were detected. The 16S rRNA sequences mainly belonged to the phyla Firmicutes (79.4%), Bacteroidetes (16.9%), Actinobacteria (2.5%), Proteobacteria (1%) and Verrumicrobia (0.1%). Interestingly, while most of OTUs appeared individual-specific, 2.1% were present in more than 50% of the samples and accounted for 35.8% of the total sequences. These 66 dominant and prevalent OTUs included members of the genera Faecalibacterium, Ruminococcus, Eubacterium, Dorea, Bacteroides, Alistipes and Bifidobacterium. Furthermore, 24 OTUs had cultured type strains representatives which should be subjected to genome sequence with a high degree of priority. Strikingly, 52 of these 66 OTUs were detected in at least three out of four recently published human faecal microbiota data sets, obtained with very different experimental procedures. A statistical model confirmed these OTUs prevalence. Despite the species richness and a high individual specificity, a limited number of OTUs is shared among individuals and might represent the phylogenetic core of the human intestinal microbiota. Its role in human health deserves further study.
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              Phylogenetic relationships of butyrate-producing bacteria from the human gut.

              Butyrate is a preferred energy source for colonic epithelial cells and is thought to play an important role in maintaining colonic health in humans. In order to investigate the diversity and stability of butyrate-producing organisms of the colonic flora, anaerobic butyrate-producing bacteria were isolated from freshly voided human fecal samples from three healthy individuals: an infant, an adult omnivore, and an adult vegetarian. A second isolation was performed on the same three individuals 1 year later. Of a total of 313 bacterial isolates, 74 produced more than 2 mM butyrate in vitro. Butyrate-producing isolates were grouped by 16S ribosomal DNA (rDNA) PCR-restriction fragment length polymorphism analysis. The results indicate very little overlap between the predominant ribotypes of the three subjects; furthermore, the flora of each individual changed significantly between the two isolations. Complete sequences of 16S rDNAs were determined for 24 representative strains and subjected to phylogenetic analysis. Eighty percent of the butyrate-producing isolates fell within the XIVa cluster of gram-positive bacteria as defined by M. D. Collins et al. (Int. J. Syst. Bacteriol. 44:812-826, 1994) and A. Willems et al. (Int. J. Syst. Bacteriol. 46:195-199, 1996), with the most abundant group (10 of 24 or 42%) clustering with Eubacterium rectale, Eubacterium ramulus, and Roseburia cecicola. Fifty percent of the butyrate-producing isolates were net acetate consumers during growth, suggesting that they employ the butyryl coenzyme A-acetyl coenzyme A transferase pathway for butyrate production. In contrast, only 1% of the 239 non-butyrate-producing isolates consumed acetate.
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                Author and article information

                Journal
                Aliment Pharmacol Ther
                Aliment. Pharmacol. Ther
                10.1111/(ISSN)1365-2036
                APT
                Alimentary Pharmacology & Therapeutics
                John Wiley and Sons Inc. (Hoboken )
                0269-2813
                1365-2036
                July 2015
                24 May 2015
                : 42
                : 2 ( doiID: 10.1111/apt.2015.42.issue-2 )
                : 158-179
                Affiliations
                [ 1 ] Department of GastroenterologyInstitute of Translational Medicine University of Liverpool LiverpoolUK
                Author notes
                [*] [* ] Correspondence to:

                Prof. B. J. Campbell, Department of Gastroenterology, Institute of Translational Medicine, University of Liverpool, Liverpool L69 3GE, UK.

                E‐mail: bjcampbl@ 123456liv.ac.uk

                Article
                APT13248
                10.1111/apt.13248
                4949558
                26011307
                76b7a813-91c1-4bae-9a78-fbfdb96c0b68
                © 2015 The Authors. Alimentary Pharmacology & Therapeutics published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 15 December 2014
                : 02 January 2015
                : 16 April 2015
                : 28 April 2015
                Page count
                Pages: 22
                Funding
                Funded by: Biotechnology and Biological Sciences Research Council
                Award ID: BB/I016783/1
                Funded by: Provexis plc
                Funded by: Bo and Vera Ax: son Johnson Foundation for Nature Medicine Limited
                Funded by: Arcis Biotechnology
                Funded by: Amgen Inc.
                Funded by: Falk Foundation
                Categories
                Review Article
                Review Article
                Custom metadata
                2.0
                apt13248
                July 2015
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.2 mode:remove_FC converted:19.07.2016

                Pharmacology & Pharmaceutical medicine
                Pharmacology & Pharmaceutical medicine

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