High-protein diet modifies colonic microbiota and luminal environment but not colonocyte metabolism in the rat model: the increased luminal bulk connection

Abstract

AM. Highprotein diet modifies colonic microbiota and luminal environment but not colonocyte metabolism in the rat model: the increased luminal bulk connection. Am J Physiol Gastrointest Liver Physiol 307: G459-G470, 2014. First published June 26, 2014; doi:10.1152/ajpgi.00400.2013.-High-protein diets are used for body weight reduction, but consequences on the large intestine ecosystem are poorly known. Here, rats were fed for 15 days with either a normoproteic diet (NP, 14% protein) or a hyperproteichypoglucidic isocaloric diet (HP, 53% protein). Cecum and colon were recovered for analysis. Short-and branched-chain fatty acids, as well as lactate, succinate, formate, and ethanol contents, were markedly increased in the colonic luminal contents of HP rats (P Ͻ 0.05 or less) but to a lower extent in the cecal luminal content. This was associated with reduced concentrations of the Clostridium coccoides and C. leptum groups and Faecalibacterium prausnitzii in both the cecum and colon (P Ͻ 0.05 or less). In addition, the microbiota diversity was found to be higher in the cecum of HP rats but was lower in the colon compared with NP rats. In HP rats, the colonic and cecal luminal content weights were markedly higher than in NP rats (P Ͻ 0.001), resulting in similar butyrate, acetate, and propionate concentrations. Accordingly, the expression of monocarboxylate transporter 1 and sodium monocarboxylate transporter 1 (which is increased by higher butyrate concentration) as well as the colonocyte capacity for butyrate oxidation were not modified by the HP diet, whereas the amount of butyrate in feces was increased (P Ͻ 0.01). It is concluded that an increased bulk in the large intestine content following HP diet consumption allows maintenance in the luminal butyrate concentration and thus its metabolism in colonocytes despite modified microbiota composition and increased substrate availability.protein; microbiota; SCFA; transport; metabolism HIGH-PROTEIN (HP) diets are commonly used for body weight loss (36,38). In fact, such diets have been shown to increase satiety, to modify lipid metabolism, and to facilitate short-and middle-term weight reduction (24,61,72). However, the consequences on gut microbiota composition, on microbial-derived metabolites in the large intestine luminal content, and on colonocyte epithelial cell metabolic capacities have been little studied.Increasing protein intake induces an increase in the proportion of nitrogenous compounds, mainly protein, peptides, and to a lesser extent amino acids, entering the large intestine (13,23,25,51,64). They are subjected to luminal proteolysis and subsequent metabolism by the large number of microorganisms of the large intestine microbiota (about 10 11 to 10 12 viable bacteria/g content) (29) leading to the production of numerous amino acid-derived metabolites (53), including phenols, indoles, amines, sulfide, ammonia, and monocarboxylic acids. Monocarboxylic acids include short-chain fatty acids (SCFA), branched-chain fatty acids (BCFA) and several other organ...

High-protein diet differently modifies intestinal goblet cell characteristics and mucosal cytokine expression in ileum and colon

“…In the ileum, we found a marked increase of the amount of acetate in the luminal content recovered from HP animals. However, and as previously found in the rat colon [10], the increased of the luminal bulk content in the small intestine of HP rats led to a similar acetate concentration in the intestinal lumen of NP and HP rats, thus allowing homeostasis of this parameter. Incidentally, the twofold increase of the amount of acetate in the small intestine luminal content after HP diet ingestion was likely due, in part at least, to an increased conversion by the small intestine microbiota of the casein-derived amino acids into this SCFA.…”

“…In ileum of HP rats, the question of a relationship between the acetate luminal content, the higher mucin production and the modifications of the ileal microbiota composition and/or activities remains open and will require further development out of the scope of the present study. Regarding this latter aspect, we have recently shown that HP diet consumption causes major changes in colonic microbiota composition, such as a significant decrease concentration of the acetate consumer Faecalibacterium prausnitzii [10], which has been shown to diminish the effects of an acetate producer bacterium on goblet cells and mucins in gnobiotic rats [31].…”

“…In the rat model, consumption of a high amount of protein markedly modifies the colonic luminal content including increased water, ammonia and short-chain fatty acids (SCFAs) content, higher protease activities in both the small and large intestines [9] and modification of the microbiota composition and diversity [10]. Numerous metabolites, depending on their luminal concentrations, are known to exert either beneficial or deleterious effects on the intestinal colonic mucosa [11].…”

Shaping functional gut microbiota using dietary bioactives to reduce colon cancer risk

“…Dietary protein levels also may influence butyrate utilization as a high protein diet has been found to decrease expression of the proton coupled monocarboxylate transporter 1 (MCT1, a butyrate transporter) in the colon of piglets [146]. In contrast, Liu et al, found no effect of dietary protein on MCT1 expression or luminal butyrate levels in rats [147]. …”

Curcumin ameliorates the tumor-enhancing effects of a high-protein diet in an azoxymethane-induced mouse model of colon carcinogenesis

“…Moreover, increased bacterial fermentation (putrefaction) of undigested protein delivered to the colon was suggested as being deleterious for the colonic epithelium through increased production of bacterial metabolites derived from amino acids including phenolic and indolic compounds, hydrogen sulfide, and branched-chain fatty acids (BCFAs; isobutyrate, isovalerate, and 2-methylbutyrate) [2,13,14]. In fact, HPD consumption markedly increased protease activities in both the small and large intestines [7] and modified microbiota composition and diversity [15].…”