Dietary Fiber-Microbiota Interactions
Dietary Fiber-Microbiota Interactions
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.
The human gut contains a dense and diverse microbial community (microbiota) and the application of affordable, modern rapid high-throughput nucleic acid sequencing technologies has transformed our understanding of its dynamic complexity. Current available metagenomic, metatranscriptomic, metaproteomic and (meta)metabolomic approaches (Table 1) and complementary bioinformatics/computational meta'omic modelling tools can now accurately characterise (albeit with some limitations) compositional changes and function/activity profiles of key microbial communities, and their interactions with the gut environment and with the host.
Initiatives such as MetaHIT (http://www.metahit.eu/) and the Human Microbiome Project (http://hmpdacc.org/) have described the composition and molecular functional profile of intestinal microbiome. On average, the healthy (normal) adult human gut microbiota consists of 10–10 micro-organisms, with the collective genome of the microbiota ('microbiome') estimated to contain 150 times as many genes than that of our own human genome with over 1000 prevalent species identified with a typical individual carrying about 160 species. The intestinal microbiota plays an important role in key nutritional, metabolic and immunological processes. It is therefore not surprising that perturbations in its composition have been implicated in many diseases and disorders, including inflammatory bowel disease (IBD), obesity and diabetes.
The intestinal microbiota becomes established in stages through early life, which begins antenatally. Interestingly, initial bacterial colonisers of the gut are largely determined by the mode of delivery; infants born naturally are initially inoculated by bacteria typically present in the vaginal and faecal microbiota, such as Lactobacillus and Prevotella spp., while those born by caesarean section are colonised by bacteria from the skin and environment. Indeed, the most significant change in microbiota composition occurs during weaning with introduction to solid foods resulting in a shift within the early 2–3 years of life towards an adult microbiota. Once established, the microbiota remains remarkably stable over time, although it has been suggested that decreased stability and altered diversity of the gut microbiota occurs with changes in body mass index (BMI) and advancing age.
In healthy adults, although the intestinal microbiota consists of several hundred bacterial species with significant inter-individual differences, over 90% present belong to the Firmicutes and Bacteroidetes, with the relative abundance of these two major phyla remaining relatively stable in health, albeit with noted large inter-individual differences in Firmicutes/Bacteroidetes ratio. Certain bacterial species are also consistently present in most individuals, indicating perhaps presence of a core microbiome. Large-scale sequence analysis had suggested that the microbial composition of all individuals, independent of their ethnicity, sex, age or body weight, might exist within three distinctive 'enterotype' clusters, predominated by Bacteroides,Prevotella or Ruminococcus spp. However, it has recently been acknowledged that Bacteroides and Ruminococcus tend to vary continuously between and within these putative 'enterotypes', challenging whether these discrete clusters are actually present and even if potential enterotype-disease associations exist, particularly given the substantial shifts observed in the microbiome in intestinal inflammation and disease. Similar intra-'enterotype' variation has also been noted for Prevotella, and even completely absent from the microbiome in some elements of the population.
While clearly the intestinal microbiota does remain stable over time, it can be significantly affected by a number of host and environmental/external factors including host genotype and immunological response, antibiotic usage, diet, and exercise. Dietary composition, modification and interventions in particular have marked impact on gut microbiota diversity, understandable given that resident micro-organisms obtain energy for growth via metabolism of dietary nutrients and the intermediate and end products of dietary fibre fermentation.
Consumption of dietary fibre significantly alters the composition of the intestinal microbiota. Hence, a greater understanding of the interaction between dietary fibre and the intestinal microbiota could represent a means of maintaining or improving the microbiota, particularly when dysbiosis exists. The aim of this review was to examine in detail the long-term and short-term impact of dietary fibre (and its various components, plant-derived polysaccharides) on the intestinal microbiota, particularly with respect to its effect on, (i) the composition of the intestinal microbiota, (ii) its role in generating short-chain fatty acids (SCFAs) – the end products of fermentation of dietary carbohydrate/fibre and energy source for the intestinal epithelium and (iii) in the context of intestinal bacteria–epithelial interactions.
Abstract and Introduction
Abstract
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.
Introduction
The human gut contains a dense and diverse microbial community (microbiota) and the application of affordable, modern rapid high-throughput nucleic acid sequencing technologies has transformed our understanding of its dynamic complexity. Current available metagenomic, metatranscriptomic, metaproteomic and (meta)metabolomic approaches (Table 1) and complementary bioinformatics/computational meta'omic modelling tools can now accurately characterise (albeit with some limitations) compositional changes and function/activity profiles of key microbial communities, and their interactions with the gut environment and with the host.
Initiatives such as MetaHIT (http://www.metahit.eu/) and the Human Microbiome Project (http://hmpdacc.org/) have described the composition and molecular functional profile of intestinal microbiome. On average, the healthy (normal) adult human gut microbiota consists of 10–10 micro-organisms, with the collective genome of the microbiota ('microbiome') estimated to contain 150 times as many genes than that of our own human genome with over 1000 prevalent species identified with a typical individual carrying about 160 species. The intestinal microbiota plays an important role in key nutritional, metabolic and immunological processes. It is therefore not surprising that perturbations in its composition have been implicated in many diseases and disorders, including inflammatory bowel disease (IBD), obesity and diabetes.
The intestinal microbiota becomes established in stages through early life, which begins antenatally. Interestingly, initial bacterial colonisers of the gut are largely determined by the mode of delivery; infants born naturally are initially inoculated by bacteria typically present in the vaginal and faecal microbiota, such as Lactobacillus and Prevotella spp., while those born by caesarean section are colonised by bacteria from the skin and environment. Indeed, the most significant change in microbiota composition occurs during weaning with introduction to solid foods resulting in a shift within the early 2–3 years of life towards an adult microbiota. Once established, the microbiota remains remarkably stable over time, although it has been suggested that decreased stability and altered diversity of the gut microbiota occurs with changes in body mass index (BMI) and advancing age.
In healthy adults, although the intestinal microbiota consists of several hundred bacterial species with significant inter-individual differences, over 90% present belong to the Firmicutes and Bacteroidetes, with the relative abundance of these two major phyla remaining relatively stable in health, albeit with noted large inter-individual differences in Firmicutes/Bacteroidetes ratio. Certain bacterial species are also consistently present in most individuals, indicating perhaps presence of a core microbiome. Large-scale sequence analysis had suggested that the microbial composition of all individuals, independent of their ethnicity, sex, age or body weight, might exist within three distinctive 'enterotype' clusters, predominated by Bacteroides,Prevotella or Ruminococcus spp. However, it has recently been acknowledged that Bacteroides and Ruminococcus tend to vary continuously between and within these putative 'enterotypes', challenging whether these discrete clusters are actually present and even if potential enterotype-disease associations exist, particularly given the substantial shifts observed in the microbiome in intestinal inflammation and disease. Similar intra-'enterotype' variation has also been noted for Prevotella, and even completely absent from the microbiome in some elements of the population.
While clearly the intestinal microbiota does remain stable over time, it can be significantly affected by a number of host and environmental/external factors including host genotype and immunological response, antibiotic usage, diet, and exercise. Dietary composition, modification and interventions in particular have marked impact on gut microbiota diversity, understandable given that resident micro-organisms obtain energy for growth via metabolism of dietary nutrients and the intermediate and end products of dietary fibre fermentation.
Consumption of dietary fibre significantly alters the composition of the intestinal microbiota. Hence, a greater understanding of the interaction between dietary fibre and the intestinal microbiota could represent a means of maintaining or improving the microbiota, particularly when dysbiosis exists. The aim of this review was to examine in detail the long-term and short-term impact of dietary fibre (and its various components, plant-derived polysaccharides) on the intestinal microbiota, particularly with respect to its effect on, (i) the composition of the intestinal microbiota, (ii) its role in generating short-chain fatty acids (SCFAs) – the end products of fermentation of dietary carbohydrate/fibre and energy source for the intestinal epithelium and (iii) in the context of intestinal bacteria–epithelial interactions.
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