Reduced Dietary Intake of Carbohydrates by Obese Subjects Results in Decreased Concentrations of Butyrate and Butyrate-Producing Bacteria in Feces

Abstract

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.Low-carbohydrate diets in which carbohydrates are largely replaced by an increased proportion of dietary protein and/or fat have proved a popular weight loss strategy for humans (1,11,36). The potential health impacts associated with increased protein (34) or fat (27) intake have been controversial among nutritionists, but less attention has been paid to the consequences of low carbohydrate supply. It has been argued that a lower carbohydrate supply may be advantageous in ameliorating insulin insensitivity (9), although this may not occur with low-glycemic-index foods (21). Furthermore, in the context of overall dietary advice consideration also needs to be given to the role of carbohydrates in maintenance of gut health and function.Dietary carbohydrates include structural polysaccharides and oligosaccharides of plant origin plus resistant starch (14, 40) that are not digested in the small intestine and, instead, enter the colon. Here they can be fermented by the microbiota of the large intestine and normally provide the main energy supply to support microbial growth in the colon. Microbial fermentation may release as much as 10% of the dietary energy, mainly in the form of short-chain fatty acids (SCFA) that also act as energy sources for host cells (46). For example, butyrate is the preferred energy source for the epithelial cells of the colon (29, 50). Furthermore, butyr...

Production of Butyrate from Lactate by a Newly Isolated Clostridium sp. BPY5

“…High concentrations of lactate are usually associated with short bowel syndrome and ulcerative colitis and can lead to neurotoxicity and cardiac arrhythmia [26]. However, lactate is detected at low levels in healthy subjects [27]. Lactate is mainly converted to other organic acids, such as butyric acid that is the preferred energy source for colonocytes and has an important role in gut health [26,28].…”

Human gut microbiota: does diet matter?

“…high-protein diet (118,119) , prebiotics (97,(120)(121)(122) , probiotics (123)(124)(125) , weight-loss diet (20,126,127) and berries (128) . More specifically, changes in the type and quantity of non-digestible carbohydrates in the human diet influence both the metabolic products formed in the lower regions of the GI tract and levels of bacterial populations detected in faeces (129) . The interactions between dietary factors, gut microbiota and host metabolism are important for maintaining homeostasis and health (130) .…”

“…In addition, it has been shown in numerous studies that as dietary carbohydrate content is reduced in the diet the count of F. prausnitzii declines, respectively (129,151) . However, some lactate-utilising bacteria within Lachnospiraceae produce less butyrate in the presence of lactate-utilising sulphate-reducing bacteria.…”

Generation of genome-scale metabolic reconstructions for 773 members of the human gut microbiota

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