Abstract
The human gastrointestinal tract is colonized by a diverse microbial community, which plays a crucial role in human health. In the gut, a protective mucus layer that consists of glycan structures separates the bacteria from the host epithelial cells. These host-derived glycans are utilized by bacteria that have adapted to this specific compound in the gastrointestinal tract. Our study investigated the close interaction between two distinct gut microbiota members known to use mucus glycans, the generalist Bacteroides thetaiotaomicron and the specialist Akkermansia muciniphila in vitro and in vivo. The in vitro study, in which mucin was the only nutrient source, indicated that B. thetaiotaomicron significantly upregulated genes coding for Glycoside Hydrolases (GHs) and mucin degradation activity when cultured in the presence of A. muciniphila. Furthermore, B. thetaiotaomicron significantly upregulated the expression of a gene encoding for membrane attack complex/perforin (MACPF) domain in co-culture. The transcriptome analysis also indicated that A. muciniphila was less affected by the environmental changes and was able to sustain its abundance in the presence of B. thetaiotaomicron while increasing the expression of LPS core biosynthesis activity encoding genes (O-antigen ligase, Lipid A and Glycosyl transferases) as well as ABC transporters. Using germ-free mice colonized with B. thetaiotaomicron and/or A. muciniphila, we observed a more general glycan degrading profile in B. thetaiotaomicron while the expression profile of A. muciniphila was not significantly affected when colonizing together, indicating that two different nutritional niches were established in mice gut. Thus, our results indicate that a mucin degrading generalist adapts to its changing environment, depending on available carbohydrates while a mucin degrading specialist adapts by coping with competing microorganism through upregulation of defense related genes.
Highlights
The gut mucosal layer is the first line of defense against damage and infection (Corfield, 2015; Bergstrom et al, 2020)
This study investigated the interaction between a mucusdegrading specialist, A. muciniphila and a mucin-degrading generalist B. thetaiotaomicron during growth in vitro and in vivo conditions
The results demonstrated that these two glycandegrading bacteria reached a stable state over time in vitro where both species co-exist and are metabolically active
Summary
The gut mucosal layer is the first line of defense against damage and infection (Corfield, 2015; Bergstrom et al, 2020). Core-glycans are covalently linked to serine or threonine residues to form complex O-linked glycan structures (Bergstrom and Xia, 2013). The type of O-glycans produced in the human intestinal tract depends on many factors encoded within the human genome, including the expression of genes responsible for mucin synthesis (MUC) (Robbe et al, 2004). The fucosyltransferase 2 (FUT2) gene is responsible for the synthesis of type 1 H antigens, whose secretion determines the expression of the ABH and Lewis histo-blood antigens in the intestinal mucosa (Wacklin et al, 2014). Bacteria that can degrade mucin glycans can colonize the mucosal surface and become core species in the gastrointestinal (GI) tract (Bergstrom and Xia, 2013; Tailford et al, 2015)
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