Abstract
BackgroundThe intestinal mucus layer plays a key role in the maintenance of host-microbiota homeostasis. To document the crosstalk between the host and microbiota, we used gnotobiotic models to study the influence of two major commensal bacteria, Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii, on this intestinal mucus layer. B. thetaiotaomicron is known to use polysaccharides from mucus, but its effect on goblet cells has not been addressed so far. F. prausnitzii is of particular physiological importance because it can be considered as a sensor and a marker of human health. We determined whether B. thetaiotaomicron affected goblet cell differentiation, mucin synthesis and glycosylation in the colonic epithelium. We then investigated how F. prausnitzii influenced the colonic epithelial responses to B. thetaiotaomicron.ResultsB. thetaiotaomicron, an acetate producer, increased goblet cell differentiation, expression of mucus-related genes and the ratio of sialylated to sulfated mucins in mono-associated rats. B. thetaiotaomicron, therefore, stimulates the secretory lineage, favoring mucus production. When B. thetaiotaomicron was associated with F. prausnitzii, an acetate consumer and a butyrate producer, the effects on goblet cells and mucin glycosylation were diminished. F. prausnitzii, by attenuating the effects of B. thetaiotaomicron on mucus, may help the epithelium to maintain appropriate proportions of different cell types of the secretory lineage. Using a mucus-producing cell line, we showed that acetate up-regulated KLF4, a transcription factor involved in goblet cell differentiation.ConclusionsB. thetaiotaomicron and F. prausnitzii, which are metabolically complementary, modulate, in vivo, the intestinal mucus barrier by modifying goblet cells and mucin glycosylation. Our study reveals the importance of the balance between two main commensal bacteria in maintaining colonic epithelial homeostasis via their respective effects on mucus.
Highlights
The intestinal mucus layer plays a key role in the maintenance of host-microbiota homeostasis
Scanning electron microscopy of cecal contents of Bt-2d (2 days after inoculation) and Bt-30d (30 days after inoculation) rats revealed B. thetaiotaomicron as short bacilli with rounded ends (Figure 1B); the bacteria were associated with luminal contents, food-residue particles and shed mucus, consistent with previous descriptions in the distal gut intestine [20]
We report that commensal bacteria can influence goblet cells and mucin composition in the gut, providing new information about the relation among mucus, bacteria and intestinal homeostasis
Summary
The intestinal mucus layer plays a key role in the maintenance of host-microbiota homeostasis. To document the crosstalk between the host and microbiota, we used gnotobiotic models to study the influence of two major commensal bacteria, Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii, on this intestinal mucus layer. Faecalibacterium prausnitzii is a Gram positive bacterium, in the Clostridium leptum group from the Firmicutes phylum These two species are metabolically complementary: B. thetaiotaomicron is an acetate producer whereas F. praunistzii is an acetate consumer and a butyrate producer [5,6]. Both are major components of the intestinal microbiota and, contribute to the interactions between the microbiota and the GIT. To establish a relevant simplified model of microbiota, we studied these two commensal bacteria as functional members of the microbiome influencing host metabolism [7]
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