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