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Open Access Research article

Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent

Laura Wrzosek123, Sylvie Miquel123, Marie-Louise Noordine123, Stephan Bouet456, Marie Joncquel Chevalier-Curt789, Véronique Robert123, Catherine Philippe1102, Chantal Bridonneau123, Claire Cherbuy123, Catherine Robbe-Masselot789, Philippe Langella123* and Muriel Thomas123*

Author Affiliations

1 INRA, UMR 1319 MICALIS, AgroParisTech, Domaine de Vilvert, Jouy-en-Josas, 78350, France

2 AgroParisTech, UMR 1319 MICALIS, Jouy-en-Josas, F-78350, France

3 Commensal and Probiotics-Host Interactions Laboratory, Jouy-en-Josas, F-78350, France

4 INRA, UMR 1313, Animal Genetics and Integrative Biology, Jouy-en-Josas, F-78350, France

5 Laboratory of Radiobiology and Genomics Studies, CEA, DSV, IRCM, SREIT, Jouy-en-Josas, F-78350, France

6 AgroParisTech, UMR 1313, Animal Genetics and Integrative Biology, Jouy-en-Josas, F-78350, France

7 Univ Lille Nord de France, Lille, F-59000, France

8 USTL, UGSF, IFR 147, CNRS, Villeneuve d’Ascq, F-59650, France

9 UMR 8576, Villeneuve d’Ascq, F-59650, France

10 Amipem Team, Jouy-en-Josas, F-78350, France

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BMC Biology 2013, 11:61  doi:10.1186/1741-7007-11-61

Published: 21 May 2013

Abstract

Background

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. 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.

Results

B. 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.

Conclusions

B. 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.

Keywords:
Germ-free rats; Goblet cells; Mucin O-glycosylation; KLF4; Short chain fatty acid