Trends in Microbiology | Microbe of the Month 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

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

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:

glycans) was later implicated.

CLASS: Bacteroidia

ORDER:

FAMILY:

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) . 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