Mucosal Glycan Foraging Enhances Fitness and Transmission of a Saccharolytic Human Gut Bacterial Symbiont

By E. Martens, Herbert C. Chiang, Jeffrey I. Gordon. Cell Host and Microbe, 2008

909 citations recorded by the source corpus.

Summary The distal human gut is a microbial bioreactor that digests complex carbohydrates. The strategies evolved by gut microbes to sense and process diverse glycans have important implications for the assembly and operations of this ecosystem. The human gut bacterium Bacteroides thetaiotaomicron forages on host and dietary glycans. Its ability to target these substrates resides in 88 polysaccharide utilization loci (PULs), encompassing 18% of its genome. In this report, whole-genome transcriptional profiling and genetic tests are used to define the mechanisms underlying host glycan foraging in vivo and in vitro. PULs that target all major classes of host glycans were identified. Mucin O-glycans are the principal substrate foraged in vivo. Simultaneous deletion of five ECF-σ transcription factors that activate mucin O-glycan utilization produces defects in bacterial persistence in the gut and in mother-to-offspring transmission. Thus, PUL-mediated glycan catabolism is an important factor in gut colonization and likely impacts gut ecology.

Subfields: Food Science, Infectious Diseases, Molecular Biology

View Paper: https://www.semanticscholar.org/paper/b8a3469b3d2a8d9a3ffdde10e2d5cc1d48f9a8c0

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Citations in the corpus

Dietary Fiber-Induced Improvement in Glucose Metabolism Is Associated with Increased Abundance of Prevotella. (2015, background): “WhileB. thetaiotaomicron utilizes a vast range of plant and animal glucans (Martens et al., 2008, 2011; Xu et al., 2003), it lacks essential genes for degradation of complex polysaccharides compared to other Bacteroides strains (Dodd et al., 2010; Martens et al., 2011).”
Microbiota in health and diseases (2022, background): “For example, Bacteroides species in the large intestine are responsible for sugar harvest.(31) Pathogenic Enterobacteriaceae also utilizes sugar and amino acids in gut.”
A dietary fiber-deprived gut microbiota degrades the colonic mucus barrier and enhances pathogen susceptibility (2016, positive): “We have previously shown that this mixture contains 110 different structures (Hickey et al., 2015) that when metabolized by B. thetaiotaomicron stimulate a transcriptional response that overlaps substantially with genes expressed in vivo under fiber-restricted conditions (Martens et al., 2008).”
Specificity of polysaccharide use in intestinal Bacteroides species determines diet-induced microbiota alterations (2010, positive): “Gene Deletion and Complementation in Bt In-frame (nonpolar) gene deletions for mutants were generated using counterselectable allele exchange (Martens et al., 2008).”
Gut Bacteroides species in health and disease (2021, background): “The Bacteroides thetaioatomicron (Bth) VPI- 5482 strain has 88 polysaccharide utilization loci (PUL) at its disposal for the degradation of various kinds of glycans including diet derived and host glycans.(14) The PUL of Bth enable it to effectively forage O-glycans during a shortage of glycans deri”
Mucin glycan foraging in the human gut microbiome (2015, background): “However, later, B. thetaiotaomicron VPI5482 was shown to be able to grow on different fractions of glycans purified from pig gastric mucosa, including an Oglycan rich fraction (Martens et al., 2008).”
Bifidobacteria or fiber protect against diet-induced microbiota-mediated colonic mucus deterioration (2017, background): “Certain microbial generalists and specialists possess various carbohydrate utilization gene clusters that allow them to degrade and metabolize specific glycans of the intestinal mucus layer (Kaoutari et al., 2013; Martens et al., 2008).”
Recognition and Degradation of Plant Cell Wall Polysaccharides by Two Human Gut Symbionts (2011, methodology): “Empirically measured in vitro substrate specificities for some PULs are labeled around each genome schematic and correspond to PULs that were induced $10-fold in response to the indicated glycan class in this or previous studies [8,12].”
Mechanisms and consequences of intestinal dysbiosis (2017, background): “thetaiotaomicron lacking polysaccharide-utilization loci involved in the metabolism of mucin O-glycans [110].”
Indoleacrylic Acid Produced by Commensal Peptostreptococcus Species Suppresses Inflammation. (2017, background): “The fucosidase and sialidase activity of certain symbiotic bacteria, such as Bacteroides thetaiotaomicron, can liberate mucosal glycans without compromising the integrity of the mucus layer to support colonization (Martens et al., 2008, 2009).”
How members of the human gut microbiota overcome the sulfation problem posed by glycosaminoglycans (2017, methodology): “Bacteroides thetaiotaomicron (Bt), a member of the CM, uses Hep and HS as high-priority nutrient sources that activate a single PUL (PULHep) (16).”
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 (2013, background): “thetaiotaomicron to grow on mucus contributes to its colonization and persistence in the GIT [18].”