Specificity of polysaccharide use in intestinal bacteroides species determines diet-induced microbiota alterations

Cell

Volumn 141, Issue 7, 2010, Pages 1241-1252

  Sonnenburg, Erica D ^a   Zheng, Hongjun ^b   Joglekar, Payal ^a   Higginbottom, Steven K ^a   Firbank, Susan J ^b   Bolam, David N ^b   Sonnenburg, Justin L ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Cellbio; Microbio

Indexed keywords

BIOCHEMICAL MARKER; FRUCTAN; FRUCTOKINASE; FRUCTOSE; GLYCOSIDASE; INULIN; LEVAN; LEVANASE; MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN; POLYSACCHARIDE; SUCROSE;

ARTICLE; BACTERIAL GROWTH; BACTEROIDES; BACTEROIDES FRAGILIS; BACTEROIDES OVATUS; BACTEROIDES THETAIOTAOMICRON; BACTEROIDES UNIFORMIS; BACTEROIDES VULGATUS; BINDING KINETICS; CARBOHYDRATE ANALYSIS; CARBOHYDRATE METABOLISM; CARBOHYDRATE SYNTHESIS; CONTROLLED STUDY; ENZYME SPECIFICITY; FOOD INTAKE; GENE LOCUS; GENE SEQUENCE; GENETIC ANALYSIS; IN VIVO STUDY; INTESTINE FLORA; NONHUMAN; PREDICTION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TWO HYBRID SYSTEM;

BACTEROIDES; BACTEROIDES THETAIOTAOMICRON;

EID: 77953901767     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2010.05.005     Document Type: Article

References (39)

1. Backhed, F., Ley, R.E., Sonnenburg, J.L., Peterson, D.A., and Gordon, J.I. (2005). Host-bacterial mutualism in the human intestine. Science (New York, NY 307, 1915-1920.
2. Bolam D.N., Xie H., Pell G., Hogg D., Galbraith G., Henrissat B., Gilbert H.J. X4 modules represent a new family of carbohydrate-binding modules that display novel properties. J. Biol. Chem. 2004, 279:22953-22963.
3. Cantarel B.L., Coutinho P.M., Rancurel C., Bernard T., Lombard V., Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2009, 37:D233-D238.
4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. 1994, 50:760-763. Collaborative Computational Project.
5. Dethlefsen L., Huse S., Sogin M.L., Relman D.A. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 2008, 6:e280.
6. Duncan S.H., Lobley G.E., Holtrop G., Ince J., Johnstone A.M., Louis P., Flint H.J. Human colonic microbiota associated with diet, obesity and weight loss. International Journal of Obesity 2008, 32:1720-1724.
7. Duncan S.H., Scott K.P., Ramsay A.G., Harmsen H.J., Welling G.W., Stewart C.S., Flint H.J. Effects of alternative dietary substrates on competition between human colonic bacteria in an anaerobic fermentor system. Appl. Environ. Microbiol. 2003, 69:1136-1142.
8. Dwyer M.A., Hellinga H.W. Periplasmic binding proteins: a versatile superfamily for protein engineering. Curr. Opin. Struct. Biol. 2004, 14:495-504.
9. Eckburg P.B., Bik E.M., Bernstein C.N., Purdom E., Dethlefsen L., Sargent M., Gill S.R., Nelson K.E., Relman D.A. Diversity of the human intestinal microbial flora. Science 2005, 308:1635-1638.
10. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. 2004, 60:2126-2132.
11. Falke J.J., Erbse A.H. The Piston Rises Again. Structure 2009, 17:1149-1152.
12. Flint H.J., Bayer E.A., Rincon M.T., Lamed R., White B.A. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nature 2008, 6:121-131.
13. Frank D.N., St Amand A.L., Feldman R.A., Boedeker E.C., Harpaz N., Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 2007, 104:13780-13785.
14. Hooper L.V. Do symbiotic bacteria subvert host immunity?. Nature 2009, 7:367-374.
15. Jernberg C., Lofmark S., Edlund C., Jansson J.K. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 2007, 1:56-66.
16. Kolida S., Meyer D., Gibson G.R. A double-blind placebo-controlled study to establish the bifidogenic dose of inulin in healthy humans. Eur. J. Clin. Nutr. 2007, 61:1189-1195.
17. Koropatkin N., Martens E.C., Gordon J.I., Smith T.J. Structure of a SusD homologue, BT1043, involved in mucin O-glycan utilization in a prominent human gut symbiont. Biochemistry 2009, 48:1532-1542.
18. Koropatkin N.M., Martens E.C., Gordon J.I., Smith T.J. Starch catabolism by a prominent human gut symbiont is directed by the recognition of amylose helices. Structure 2008, 16:1105-1115.
19. Leslie A.G.W. Recent changes to the MOSFLM package for processing film and image plate data. Joint CCP4 + ESF-EAMCB Newsletter on Protein Crystallography 1992, 26.
20. Ley R.E., Turnbaugh P.J., Klein S., Gordon J.I. Microbial ecology: human gut microbes associated with obesity. Nature 2006, 444:1022-1023.
21. Louis P., Scott K.P., Duncan S.H., Flint H.J. Understanding the effects of diet on bacterial metabolism in the large intestine. J. Appl. Microbiol. 2007, 102:1197-1208.
22. Lozupone C.A., Hamady M., Cantarel B.L., Coutinho P.M., Henrissat B., Gordon J.I., Knight R. The convergence of carbohydrate active gene repertoires in human gut microbes. Proc. Natl. Acad. Sci. USA 2008, 105:15076-15081.
23. Martens E.C., Chiang H.C., Gordon J.I. Mucosal glycan foraging enhances fitness and transmission of a saccharolytic human gut bacterial symbiont. Cell Host Microbe 2008, 4:447-457.
24. Martens E.C., Koropatkin N.M., Smith T.J., Gordon J.I. Complex glycan catabolism by the human gut microbiota: The bacteroidetes Sus-like paradigm. J. Biol. Chem. 2009, 284:24673-24677.
25. Menne E., Guggenbuhl N., Roberfroid M. Fn-type chicory inulin hydrolysate has a prebiotic effect in humans. J. Nutr. 2000, 130:1197-1199.
26. Miller G.L. Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar. Anal. Chem. 1959, 31:426-428.
27. Ramirez-Farias C., Slezak K., Fuller Z., Duncan A., Holtrop G., Louis P. Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br. J. Nutr. 2008, 101:541-550.
28. Roberfroid M., Gibson G.R., Delzenne N. The biochemistry of oligofructose, a nondigestible fiber: an approach to calculate its caloric value. Nutr. Rev. 1993, 51:137-146.
29. Rossi M., Corradini C., Amaretti A., Nicolini M., Pompei A., Zanoni S., Matteuzzi D. Fermentation of fructooligosaccharides and inulin by bifidobacteria: a comparative study of pure and fecal cultures. Appl. Environ. Microbiol. 2005, 71:6150-6158.
30. Samuel B.S., Gordon J.I. A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc. Natl. Acad. Sci. USA 2006, 103:10011-10016.
31. Shipman J.A., Berleman J.E., Salyers A.A. Characterization of four outer membrane proteins involved in binding starch to the cell surface of Bacteroides thetaiotaomicron. J. Bacteriol. 2000, 182:5365-5372.
32. Sonnenburg E.D., Sonnenburg J.L., Manchester J.K., Hansen E.E., Chiang H.C., Gordon J.I. A hybrid two-component system protein of a prominent human gut symbiont couples glycan sensing in vivo to carbohydrate metabolism. Proc. Natl. Acad. Sci. USA 2006, 103:8834-8839.
33. Sonnenburg J.L., Xu J., Leip D.D., Chen C.H., Westover B.P., Weatherford J., Buhler J.D., Gordon J.I. Glycan foraging in vivo by an intestine-adapted bacterial symbiont. Science 2005, 307:1955-1959.
34. Turnbaugh P.J., Hamady M., Yatsunenko T., Cantarel B.L., Duncan A., Ley R.E., Sogin M.L., Jones W.J., Roe B.A., Affourtit J.P., et al. A core gut microbiome in obese and lean twins. Nature 2009, 457:480-484.
35. Turnbaugh P.J., Ley R.E., Hamady M., Fraser-Liggett C.M., Knight R., Gordon J.I. The human microbiome project. Nature 2007, 449:804-810.
36. Van der Meulen R., Makras L., Verbrugghe K., Adriany T., De Vuyst L. In vitro kinetic analysis of oligofructose consumption by Bacteroides and Bifidobacterium spp. indicates different degradation mechanisms. Appl. Environ. Microbiol. 2006, 72:1006-1012.
37. Westover B.P., Buhler J.D., Sonnenburg J.L., Gordon J.I. Operon prediction without a training set. Bioinformatics 2005, 21:880-888.
38. Xu J., Bjursell M.K., Himrod J., Deng S., Carmichael L.K., Chiang H.C., Hooper L.V., Gordon J.I. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 2003, 299:2074-2076.
39. Xu J., Mahowald M.A., Ley R.E., Lozupone C.A., Hamady M., Martens E.C., Henrissat B., Coutinho P.M., Minx P., Latreille P., et al. Evolution of Symbiotic Bacteria in the Distal Human Intestine. PLoS Biol. 2007, 5:e156.