Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Science 25 March 2005:
Vol. 307. no. 5717, pp. 1955 - 1959
DOI: 10.1126/science.1109051
Prev | Table of Contents | Next

Reports

Glycan Foraging in Vivo by an Intestine-Adapted Bacterial Symbiont

Justin L. Sonnenburg,1,2 Jian Xu,1,2 Douglas D. Leip,1,2 Chien-Huan Chen,1,2 Benjamin P. Westover,1,3 Jeremy Weatherford,3 Jeremy D. Buhler,1,3 Jeffrey I. Gordon1,2*

Germ-free mice were maintained on polysaccharide-rich or simple-sugar diets and colonized for 10 days with an organism also found in human guts, Bacteroides thetaiotaomicron, followed by whole-genome transcriptional profiling of bacteria and mass spectrometry of cecal glycans. We found that these bacteria assembled on food particles and mucus, selectively induced outer-membrane polysaccharide-binding proteins and glycoside hydrolases, prioritized the consumption of liberated hexose sugars, and revealed a capacity to turn to host mucus glycans when polysaccharides were absent from the diet. This flexible foraging behavior should contribute to ecosystem stability and functional diversity.

1 Center for Genome Sciences, Washington University, St. Louis, MO 63108, USA.
2 Department of Molecular Biology and Pharmacology, Washington University, St. Louis, MO 63108, USA.
3 Department of Computer Science and Engineering, Washington University, St. Louis, MO 63108, USA.

* To whom correspondence should be addressed. E-mail: jgordon{at}molecool.wustl.edu

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Crystal Structure of a Mucus-binding Protein Repeat Reveals an Unexpected Functional Immunoglobulin Binding Activity.
D. A. MacKenzie, L. E. Tailford, A. M. Hemmings, and N. Juge (2009)
J. Biol. Chem. 284, 32444-32453
   Abstract »    Full Text »    PDF »
Identification of the Site-Specific DNA Invertase Responsible for the Phase Variation of SusC/SusD Family Outer Membrane Proteins in Bacteroides fragilis.
H. Nakayama-Imaohji, H. Hirakawa, M. Ichimura, S. Wakimoto, S. Kuhara, T. Hayashi, and T. Kuwahara (2009)
J. Bacteriol. 191, 6003-6011
   Abstract »    Full Text »    PDF »
Complex Glycan Catabolism by the Human Gut Microbiota: The Bacteroidetes Sus-like Paradigm.
E. C. Martens, N. M. Koropatkin, T. J. Smith, and J. I. Gordon (2009)
J. Biol. Chem. 284, 24673-24677
   Abstract »    Full Text »    PDF »
The core gut microbiome, energy balance and obesity.
P. J. Turnbaugh and J. I. Gordon (2009)
J. Physiol. 587, 4153-4158
   Abstract »    Full Text »    PDF »
Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation.
P. A. Crawford, J. R. Crowley, N. Sambandam, B. D. Muegge, E. K. Costello, M. Hamady, R. Knight, and J. I. Gordon (2009)
PNAS 106, 11276-11281
   Abstract »    Full Text »    PDF »
Coordinate Regulation of Glycan Degradation and Polysaccharide Capsule Biosynthesis by a Prominent Human Gut Symbiont.
E. C. Martens, R. Roth, J. E. Heuser, and J. I. Gordon (2009)
J. Biol. Chem. 284, 18445-18457
   Abstract »    Full Text »    PDF »
Mixed-Species Genomic Microarray Analysis of Fecal Samples Reveals Differential Transcriptional Responses of Bifidobacteria in Breast- and Formula-Fed Infants.
E. S. Klaassens, R. J. Boesten, M. Haarman, J. Knol, F. H. Schuren, E. E. Vaughan, and W. M. de Vos (2009)
Appl. Envir. Microbiol. 75, 2668-2676
   Abstract »    Full Text »    PDF »
Coculture Fermentations of Bifidobacterium Species and Bacteroides thetaiotaomicron Reveal a Mechanistic Insight into the Prebiotic Effect of Inulin-Type Fructans.
G. Falony, T. Calmeyn, F. Leroy, and L. De Vuyst (2009)
Appl. Envir. Microbiol. 75, 2312-2319
   Abstract »    Full Text »    PDF »
Characterizing a model human gut microbiota composed of members of its two dominant bacterial phyla.
M. A. Mahowald, F. E. Rey, H. Seedorf, P. J. Turnbaugh, R. S. Fulton, A. Wollam, N. Shah, C. Wang, V. Magrini, R. K. Wilson, et al. (2009)
PNAS 106, 5859-5864
   Abstract »    Full Text »    PDF »
Enterotoxigenic Bacteroides fragilis: a Rogue among Symbiotes.
C. L. Sears (2009)
Clin. Microbiol. Rev. 22, 349-369
   Abstract »    Full Text »    PDF »
The Human Intestinal Microbiome: A New Frontier of Human Biology.
M. Hattori and T. D. Taylor (2009)
DNA Res 16, 1-12
   Abstract »    Full Text »    PDF »
Effects of the gut microbiota on host adiposity are modulated by the short-chain fatty-acid binding G protein-coupled receptor, Gpr41.
B. S. Samuel, A. Shaito, T. Motoike, F. E. Rey, F. Backhed, J. K. Manchester, R. E. Hammer, S. C. Williams, J. Crowley, M. Yanagisawa, et al. (2008)
PNAS 105, 16767-16772
   Abstract »    Full Text »    PDF »
The convergence of carbohydrate active gene repertoires in human gut microbes.
C. A. Lozupone, M. Hamady, B. L. Cantarel, P. M. Coutinho, B. Henrissat, J. I. Gordon, and R. Knight (2008)
PNAS 105, 15076-15081
   Abstract »    Full Text »    PDF »
Verminephrobacter eiseniae gen. nov., sp. nov., a nephridial symbiont of the earthworm Eisenia foetida (Savigny).
N. Pinel, S. K. Davidson, and D. A. Stahl (2008)
Int J Syst Evol Microbiol 58, 2147-2157
   Abstract »    Full Text »    PDF »
Modulation of Intestinal Goblet Cell Function during Infection by an Attaching and Effacing Bacterial Pathogen.
K. S. B. Bergstrom, J. A. Guttman, M. Rumi, C. Ma, S. Bouzari, M. A. Khan, D. L. Gibson, A. W. Vogl, and B. A. Vallance (2008)
Infect. Immun. 76, 796-811
   Abstract »    Full Text »    PDF »
Gene Expression of Commensal Lactobacillus johnsonii Strain NCC533 during In Vitro Growth and in the Murine Gut.
E. Denou, B. Berger, C. Barretto, J.-M. Panoff, F. Arigoni, and H. Brussow (2007)
J. Bacteriol. 189, 8109-8119
   Abstract »    Full Text »    PDF »
Bacteroides: the Good, the Bad, and the Nitty-Gritty.
H. M. Wexler (2007)
Clin. Microbiol. Rev. 20, 593-621
   Abstract »    Full Text »    PDF »
Functional Genomic Studies of Uropathogenic Escherichia coli and Host Urothelial Cells when Intracellular Bacterial Communities Are Assembled.
C. S. Reigstad, S. J. Hultgren, and J. I. Gordon (2007)
J. Biol. Chem. 282, 21259-21267
   Abstract »    Full Text »    PDF »
Genomic and metabolic adaptations of Methanobrevibacter smithii to the human gut.
B. S. Samuel, E. E. Hansen, J. K. Manchester, P. M. Coutinho, B. Henrissat, R. Fulton, P. Latreille, K. Kim, R. K. Wilson, and J. I. Gordon (2007)
PNAS 104, 10643-10648
   Abstract »    Full Text »    PDF »
Functional Genomic Studies of the Intestinal Response to a Foodborne Enteropathogen in a Humanized Gnotobiotic Mouse Model.
M. Lecuit, J. L. Sonnenburg, P. Cossart, and J. I. Gordon (2007)
J. Biol. Chem. 282, 15065-15072
   Abstract »    Full Text »    PDF »
Evolution of carbohydrate antigens--microbial forces shaping host glycomes?.
J. R. Bishop and P. Gagneux (2007)
Glycobiology 17, 23R-34R
   Abstract »    Full Text »    PDF »
In vivo imaging and genetic analysis link bacterial motility and symbiosis in the zebrafish gut.
J. F. Rawls, M. A. Mahowald, A. L. Goodman, C. M. Trent, and J. I. Gordon (2007)
PNAS 104, 7622-7627
   Abstract »    Full Text »    PDF »
Mannose Foraging by Bacteroides thetaiotaomicron: STRUCTURE AND SPECIFICITY OF THE beta-MANNOSIDASE, BtMan2A.
L. E. Tailford, V. A. Money, N. L. Smith, C. Dumon, G. J. Davies, and H. J. Gilbert (2007)
J. Biol. Chem. 282, 11291-11299
   Abstract »    Full Text »    PDF »
Spatial and Temporal Population Dynamics of a Naturally Occurring Two-Species Microbial Community inside the Digestive Tract of the Medicinal Leech.
Y. Kikuchi and J. Graf (2007)
Appl. Envir. Microbiol. 73, 1984-1991
   Abstract »    Full Text »    PDF »
Spatial and Temporal Expression of Lactobacillus plantarum Genes in the Gastrointestinal Tracts of Mice.
M. L. Marco, R. S. Bongers, W. M. de Vos, and M. Kleerebezem (2007)
Appl. Envir. Microbiol. 73, 124-132
   Abstract »    Full Text »    PDF »
Functional Genomic and Metabolic Studies of the Adaptations of a Prominent Adult Human Gut Symbiont, Bacteroides thetaiotaomicron, to the Suckling Period.
M. K. Bjursell, E. C. Martens, and J. I. Gordon (2006)
J. Biol. Chem. 281, 36269-36279
   Abstract »    Full Text »    PDF »
Characterization of the Primary Starch Utilization Operon in the Obligate Anaerobe Bacteroides fragilis: Regulation by Carbon Source and Oxygen.
C. Spence, W. G. Wells, and C. J. Smith (2006)
J. Bacteriol. 188, 4663-4672
   Abstract »    Full Text »    PDF »
A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism.
B. S. Samuel and J. I. Gordon (2006)
PNAS 103, 10011-10016
   Abstract »    Full Text »    PDF »
A hybrid two-component system protein of a prominent human gut symbiont couples glycan sensing in vivo to carbohydrate metabolism.
E. D. Sonnenburg, J. L. Sonnenburg, J. K. Manchester, E. E. Hansen, H. C. Chiang, and J. I. Gordon (2006)
PNAS 103, 8834-8839
   Abstract »    Full Text »    PDF »
Unexpected diversity and complexity of the guerrero negro hypersaline microbial mat..
R. E. Ley, J. K. Harris, J. Wilcox, J. R. Spear, S. R. Miller, B. M. Bebout, J. A. Maresca, D. A. Bryant, M. L. Sogin, and N. R. Pace (2006)
Appl. Envir. Microbiol. 72, 3685-3695
   Abstract »    Full Text »    PDF »
Characterization of Bacteroides fragilis Hemolysins and Regulation and Synergistic Interactions of HlyA and HlyB.
K. P. Robertson, C. J. Smith, A. M. Gough, and E. R. Rocha (2006)
Infect. Immun. 74, 2304-2316
   Abstract »    Full Text »    PDF »
Comparative analysis of proteins with a mucus-binding domain found exclusively in lactic acid bacteria.
J. Boekhorst, Q. Helmer, M. Kleerebezem, and R. J. Siezen (2006)
Microbiology 152, 273-280
   Abstract »    Full Text »    PDF »
A Novel Bacterial Mucinase, Glycosulfatase, Is Associated with Bacterial Vaginosis.
A. M. Roberton, R. Wiggins, P. J. Horner, R. Greenwood, T. Crowley, A. Fernandes, M. Berry, and A. P. Corfield (2005)
J. Clin. Microbiol. 43, 5504-5508
   Abstract »    Full Text »    PDF »
Epithelial Cells and Their Neighbors. IV. Bacterial contributions to intestinal epithelial barrier integrity.
A. S. Ismail and L. V. Hooper (2005)
Am J Physiol Gastrointest Liver Physiol 289, G779-G784
   Abstract »    Full Text »    PDF »
Obesity alters gut microbial ecology.
R. E. Ley, F. Backhed, P. Turnbaugh, C. A. Lozupone, R. D. Knight, and J. I. Gordon (2005)
PNAS 102, 11070-11075
   Abstract »    Full Text »    PDF »
Host-Bacterial Mutualism in the Human Intestine.
F. Backhed, R. E. Ley, J. L. Sonnenburg, D. A. Peterson, and J. I. Gordon (2005)
Science 307, 1915-1920
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)