Abstract
ABSTRACTAncestral human populations had diets containing more indigestible plant material than present-day diets in industrialized countries. One hypothesis for the rise in prevalence of obesity is that physiological mechanisms for controlling appetite evolved to match a diet with plant fiber content higher than that of present-day diets. We investigated how diet affects gut microbiota and colon cells by comparing human microbial communities with those from a primate that has an extreme plant-based diet, namely, the gelada baboon, which is a grazer. The effects of potato (high starch) versus grass (high lignin and cellulose) diets on human-derived versus gelada-derived fecal communities were compared in vitro. We especially focused on the production of short-chain fatty acids, which are hypothesized to be key metabolites influencing appetite regulation pathways. The results confirmed that diet has a major effect on bacterial numbers, short-chain fatty acid production, and the release of hormones involved in appetite suppression. The potato diet yielded greater production of short-chain fatty acids and hormone release than the grass diet, even in the gelada cultures, which we had expected should be better adapted to the grass diet. The strong effects of diet on hormone release could not be explained, however, solely by short-chain fatty acid concentrations. Nuclear magnetic resonance spectroscopy found changes in additional metabolites, including betaine and isoleucine, that might play key roles in inhibiting and stimulating appetite suppression pathways. Our study results indicate that a broader array of metabolites might be involved in triggering gut hormone release in humans than previously thought.
Highlights
Obesity, the health consequences of obesity, and the associated morbidity are major public health issues for western populations [1]
We estimated the densities of total bacteria and 5 functionally important taxa using fluorescence in-situ hybridization (FISH) (Materials and Methods; see Table S1 in the supplemental material for a description of the taxonomic range covered by each primer set)
In the case of bifidobacteria, an important taxon degrading plant starch and other fibers, it was recently reported that standard primers used in 16S sequencing led to underrepresentation of this genus [21]
Summary
The health consequences of obesity, and the associated morbidity are major public health issues for western populations [1]. It is likely that such diets generated large amounts of materials, such as lignin and cellulose, that escape digestion in the upper gut Much of this material can be fermented by the colonic microbiota to a number of products, including short-chain fatty acids (SCFA). Of particular interest is the recent description of a large number of nutrient-sensing G protein-coupled receptors on the apical surface of the neuroendocrine L cell [12] This cell secretes anorectic gut hormones such as peptide YY (PYY) and glucagon-likepeptide-1 (GLP-1) [13]. Native to the highlands of Ethiopia, these animals subsist largely as grazers, the only modern primate species to do so The remains of their fossilized ancestors displayed isotope ratios indicative of C4 plant dietary components equivalent to those seen with some lineages of early hominins [8]. Comparing the capacities of gelada microbiota and human microbiota to extract energy from energy-poor diets and to generate metabolites that feed into gut hormone pathways might provide insights into the potential consequence of energy-poor diets in ancestral hominins for gut signaling pathways
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