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      Review article: dietary fibre–microbiota interactions

      1 , , 1

      Alimentary Pharmacology & Therapeutics

      John Wiley and Sons Inc.

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          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          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 references 111

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          A human gut microbial gene catalogue established by metagenomic sequencing.

          To understand the impact of gut microbes on human health and well-being it is crucial to assess their genetic potential. Here we describe the Illumina-based metagenomic sequencing, assembly and characterization of 3.3 million non-redundant microbial genes, derived from 576.7 gigabases of sequence, from faecal samples of 124 European individuals. The gene set, approximately 150 times larger than the human gene complement, contains an overwhelming majority of the prevalent (more frequent) microbial genes of the cohort and probably includes a large proportion of the prevalent human intestinal microbial genes. The genes are largely shared among individuals of the cohort. Over 99% of the genes are bacterial, indicating that the entire cohort harbours between 1,000 and 1,150 prevalent bacterial species and each individual at least 160 such species, which are also largely shared. We define and describe the minimal gut metagenome and the minimal gut bacterial genome in terms of functions present in all individuals and most bacteria, respectively.
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            A core gut microbiome in obese and lean twins

            The human distal gut harbors a vast ensemble of microbes (the microbiota) that provide us with important metabolic capabilities, including the ability to extract energy from otherwise indigestible dietary polysaccharides1–6. Studies of a small number of unrelated, healthy adults have revealed substantial diversity in their gut communities, as measured by sequencing 16S rRNA genes6–8, yet how this diversity relates to function and to the rest of the genes in the collective genomes of the microbiota (the gut microbiome) remains obscure. Studies of lean and obese mice suggest that the gut microbiota affects energy balance by influencing the efficiency of calorie harvest from the diet, and how this harvested energy is utilized and stored3–5. To address the question of how host genotype, environmental exposures, and host adiposity influence the gut microbiome, we have characterized the fecal microbial communities of adult female monozygotic and dizygotic twin pairs concordant for leanness or obesity, and their mothers. Analysis of 154 individuals yielded 9,920 near full-length and 1,937,461 partial bacterial 16S rRNA sequences, plus 2.14 gigabases from their microbiomes. The results reveal that the human gut microbiome is shared among family members, but that each person’s gut microbial community varies in the specific bacterial lineages present, with a comparable degree of co-variation between adult monozygotic and dizygotic twin pairs. However, there was a wide array of shared microbial genes among sampled individuals, comprising an extensive, identifiable ‘core microbiome’ at the gene, rather than at the organismal lineage level. Obesity is associated with phylum-level changes in the microbiota, reduced bacterial diversity, and altered representation of bacterial genes and metabolic pathways. These results demonstrate that a diversity of organismal assemblages can nonetheless yield a core microbiome at a functional level, and that deviations from this core are associated with different physiologic states (obese versus lean).
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              Diet rapidly and reproducibly alters the human gut microbiome

              Long-term diet influences the structure and activity of the trillions of microorganisms residing in the human gut 1–5 , but it remains unclear how rapidly and reproducibly the human gut microbiome responds to short-term macronutrient change. Here, we show that the short-term consumption of diets composed entirely of animal or plant products alters microbial community structure and overwhelms inter-individual differences in microbial gene expression. The animal-based diet increased the abundance of bile-tolerant microorganisms (Alistipes, Bilophila, and Bacteroides) and decreased the levels of Firmicutes that metabolize dietary plant polysaccharides (Roseburia, Eubacterium rectale, and Ruminococcus bromii). Microbial activity mirrored differences between herbivorous and carnivorous mammals 2 , reflecting trade-offs between carbohydrate and protein fermentation. Foodborne microbes from both diets transiently colonized the gut, including bacteria, fungi, and even viruses. Finally, increases in the abundance and activity of Bilophila wadsworthia on the animal-based diet support a link between dietary fat, bile acids, and the outgrowth of microorganisms capable of triggering inflammatory bowel disease 6 . In concert, these results demonstrate that the gut microbiome can rapidly respond to altered diet, potentially facilitating the diversity of human dietary lifestyles.
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                Author and article information

                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

                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
                APT13248
                10.1111/apt.13248
                4949558
                26011307
                © 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.

                Counts
                Pages: 22
                Product
                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

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