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Bacteroides Thetaiotaomicron Trends in Microbiology | Microbe of the Month Bacteroides thetaiotaomicron 1 1 1,* Nathan T. Porter, Ana S. Luis, and Eric C. Martens 1 University of Michigan Medical School, Ann Arbor, MI 48109, USA Dynamic cell surface KEY FACTS: Nonmotile, obligate anaerobe first Outer membrane Phase variaƟon of CPS types LPS modificaƟon Phase-variable, Sus-like systems vesicles (OMVs) complement symbols: cultured and named Bacillus resistant S-layer SusCD-like proteins thetaiotaomicron by Arcangelo Distaso Surface glycan in 1912 because cell morphologies binding proteins B AMP- LpxF AMP- (phosphatase) sensiƟve resistant Cell surface and resemble the three Greek letters (u i ). LPS LPS periplasmic enzymes Largely found in humans, although cow, pig, goat, and mouse isolates Up to 9 CPS BT1927 (S-layer “ON”) loci / strain: have been recovered. Promoter inversion BT1927 (S-layer “OFF”) Acetate The first common human gut bacterium Lactate to be developed as a genetically FermentaƟon Glycolysis tractable model to study carbohydrate Coordinate regulaƟon of capsules by host glycans Succinate Propionate digestion by Abigail Salyers and coworkers. Cytoplasm One of the first human gut symbionts to have its genome fully sequenced by Periplasm Jeffrey Gordon and coworkers and to Sugar symbols: -glucose -xylose M methyl be analyzed using functional genomics -galactose ½-arabinose A acetyl in gnotobiotic mice fed different diets. Unused -GlcNAc ½-rhamnose B borate -GalNAc -DHA -NeuNAc -KDO When introduced into germ-free mice Starch and glycogen ½-fucose -apiose Bt (starch uƟlizaƟon system) Host mucus glycans Complex pecƟns lacking a complex microbiome, -galacturonic acid ½-aceric acid alone initiates epithelial and Polysaccharide metabolism -glucuronic acid ½-galactose immunological development, such as expression of fucosylated glycans in This infographic on Bacteroides thetaiotaomicron (Bt) explores the ability of this microbe to digest a broad array the ileum. of complex carbohydrates, alter its surface features, and its emerging role in gastrointestinal diseases. The infographic of Bacteroides thetaiotaomicron (Bt) illustrates two key facets of its symbiotic lifestyle in the While it is capable of depolymerizing a fi human gut: a broad ability to digest dietary fiber polysaccharides and host glycans, and a dynamic cell-surface broad range of dietary ber architecture that promotes both interactions with and evasion of the host immune system. The starch-utilization polysaccharides, it also harbors an system (Sus) is a cell-surface and periplasmic system involved in starch cleavage and transport. Over 80 extensive enzymatic apparatus for additional Sus-like systems utilize substrates ranging from host glycans to plant cell wall pectins. Bt has evolved foraging on host glycans, including N O intricate strategies to interact with other microbes or its host, including modification of its surface. Some nutrient both - and -linked glycans utilization pathways select for or directly trigger changes in capsular polysaccharide (CPS) expression. Like other contained in host cells and secreted fermentative members of the gut microbiome, Bt produces host absorbable short-chain and organic acids, mucus. which can all be absorbed by the host as a source of energy. One of the first human gut commensal bacteria for which Koch’s postulates was fulfilled in a murine model of TAXONOMY: inflammatory bowel disease, and an KINGDOM: Bacteria underlying pathway (desulfation of host PHYLUM: Bacteroidetes glycans) was later implicated. CLASS: Bacteroidia ORDER: Bacteroidales FAMILY: Bacteroidaceae GENUS: Bacteroides SPECIES: thetaiotaomicron Gram-negative *Correspondence: [email protected] (E.C. Martens). Trends in Microbiology, Month Year, Vol. xx, No. yy © 2018 Elsevier Ltd. All rights reserved. https://doi.org/10.1016/j.tim.2018.08.005 1 Trends in Microbiology | Microbe of the Month Acknowledgments The original drawing of Bacteroides thetaiotaomicron (then called Bacillus thetaiotaomicron) is reprinted from Distaso (1912). Literature 1. Distaso, A. (1912) Contribution à l'étude sur l'intoxication intestinale. Centralbl. Bakteriol. Parasit. Orig. 62, 433 2. Anderson, K.L. and Salyers, A.A. (1989) Genetic evidence that outer membrane binding of starch is required for starch utilization by Bacteroides thetaiotaomicron. J. Bacteriol. 171, 3199–3204 3. Sonnenburg, J.L. et al. (2005) Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 307, 1955–1959 4. Porter, N.T. and Martens, E.C. (2017) The critical roles of polysaccharides in gut microbial ecology and physiology. Annu. Rev. Microbiol. 71, 349–369 5. Hickey, C.A. et al. (2015) Colitogenic Bacteroides thetaiotaomicron antigens access host immune cells in a sulfatase-dependent manner via outer membrane vesicles. Cell Host Microbe 17, 672–680 6. Porter, N.T. et al. (2017) A subset of polysaccharide capsules in the human symbiont Bacteroides thetaiotaomicron promote increased competitive fitness in the mouse gut. Cell Host Microbe 22, 494–506 7. Ng, K.M. et al. (2013) Microbiota-liberated host sugars facilitate post-antibiotic expansion of enteric pathogens. Nature 502, 96–99 8. Cullen, T.W. et al. (2015) Gut microbiota. Antimicrobial peptide resistance mediates resilience of prominent gut commensals during inflammation. Science 347, 170–175 9. Taketani, M. et al. (2015) A phase-variable surface layer from the gut symbiont Bacteroides thetaiotaomicron. mBio 6, e01339-15 10. Luis, A.S. et al. (2018) Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides. Nat. Microbiol. 3, 210–219 2 Trends in Microbiology, Month Year, Vol. xx, No. yy © 2018 Elsevier Ltd. All rights reserved. https://doi.org/10.1016/j.tim.2018.08.005.
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