Introduction/Rationale: The complex polysaccharides present in dietary fiber are the major carbon source for several members of the microbiota and therefore changes in its consumption impact the microbiota composition and its interaction with the immune system. Despite this, the impact of fiber consumption on intestinal immunity is largely unknown.
Methods: Using flow cytometry, RNA-seq and metagenomics, in animal models receiving modified diets with low or standard fiber content,
Results: we show that a low fiber diet (LFF) changes the small intestinal (SI) microbiota composition and impairs SI Th17, and intraepithelial (IEL) T cell development. T cell development is restored with dietary fiber supplementation, but this defect became persistent when mice were fed LFF diets over generations. In these mice, only a microbiota transplant and a fiber-rich diet can restore T cell development. Analyzing the microbiota, we identified that a LFF diet reduces segmented filamentous bacteria (SFB) abundance. Moreover, we discovered that SFB supports the development of IELs by inducing the secretion of IFNg by type 1 innate lymphoid cells (ILC1s) needed for MHC-II upregulation on intestinal epithelial cells (IECs). We discovered that MHC-II antigen presentation by IECs is required for the development of CD4+CD8αα+ intraepithelial lymphocytes (DP IELs). Finally, we show that a low fiber diet reduces SFB abundance in the SI by promoting overgrowth of another microbiota member, Bifidobacterium pseudolongum which antagonizes SFB growth.
Conclusion: Collectively we highlight the importance of dietary fiber in maintaining the balance among microbiota members that allow IEC MHC-II antigen presentation and define a mechanism of microbiota-ILC-IEC interactions needed for the development of intestinal intraepithelial T cells.
