Specificity of Polysaccharide Use in Intestinal Bacteroides Species Determines Diet-induced Microbiota Alterations

Overview

Journal Cell

Publisher Cell Press

Specialty Cell Biology

Date 2010 Jul 7

PMID 20603004

Citations 340

Authors

Erica D Sonnenburg

Hongjun Zheng

Payal Joglekar

Steven K Higginbottom

Susan J Firbank

David N Bolam

Justin L Sonnenburg

Affiliations

Soon will be listed here.

Abstract

The intestinal microbiota impacts many facets of human health and is associated with human diseases. Diet impacts microbiota composition, yet mechanisms that link dietary changes to microbiota alterations remain ill-defined. Here we elucidate the basis of Bacteroides proliferation in response to fructans, a class of fructose-based dietary polysaccharides. Structural and genetic analysis disclosed a fructose-binding, hybrid two-component signaling sensor that controls the fructan utilization locus in Bacteroides thetaiotaomicron. Gene content of this locus differs among Bacteroides species and dictates the specificity and breadth of utilizable fructans. BT1760, an extracellular beta2-6 endo-fructanase, distinguishes B. thetaiotaomicron genetically and functionally, and enables the use of the beta2-6-linked fructan levan. The genetic and functional differences between Bacteroides species are predictive of in vivo competitiveness in the presence of dietary fructans. Gene sequences that distinguish species' metabolic capacity serve as potential biomarkers in microbiomic datasets to enable rational manipulation of the microbiota via diet.

Citing Articles

Dietary content and eating behavior in ulcerative colitis: a narrative review and future perspective.

Qin L, Lv W Nutr J. 2025; 24(1):12.

PMID: 39849464 PMC: 11755847. DOI: 10.1186/s12937-025-01075-y.

The global RNA-binding protein RbpB is a regulator of polysaccharide utilization in Bacteroides thetaiotaomicron.

Ruttiger A, Ryan D, Spiga L, Lamm-Schmidt V, Prezza G, Reichardt S Nat Commun. 2025; 16(1):208.

PMID: 39747016 PMC: 11697453. DOI: 10.1038/s41467-024-55383-8.

Polymerization of dietary fructans differentially affects interactions among intestinal microbiota of colitis mice.

Xiao Y, Zhao Q, Ni D, Zhang X, Hao W, Yuan Q ISME J. 2025; 19(1.

PMID: 39745882 PMC: 11742283. DOI: 10.1093/ismejo/wrae262.

Stable isotope fingerprinting can directly link intestinal microorganisms with their carbon source and captures diet-induced substrate switching .

Mordant A, Blakeley-Ruiz J, Kleiner M bioRxiv. 2024; .

PMID: 39713332 PMC: 11661160. DOI: 10.1101/2024.12.10.627769.

Identification of novel fructo-oligosaccharide bacterial consumers by pulse metatranscriptomics in a human stool sample.

Prattico C, Gonzalez E, Dridi L, Jazestani S, Low K, Abbott D mSphere. 2024; 10(1):e0066824.

PMID: 39699190 PMC: 11774028. DOI: 10.1128/msphere.00668-24.

References

. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr. 1994; 50(Pt 5):760-3. DOI: 10.1107/S0907444994003112. View

Samuel B, Gordon J . A humanized gnotobiotic mouse model of host-archaeal-bacterial mutualism. Proc Natl Acad Sci U S A. 2006; 103(26):10011-6. PMC: 1479766. DOI: 10.1073/pnas.0602187103. View

Xu J, Bjursell M, Himrod J, Deng S, Carmichael L, Chiang H . A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science. 2003; 299(5615):2074-6. DOI: 10.1126/science.1080029. View

Dethlefsen L, Huse S, Sogin M, Relman D . The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 2008; 6(11):e280. PMC: 2586385. DOI: 10.1371/journal.pbio.0060280. View

Ley R, Turnbaugh P, Klein S, Gordon J . Microbial ecology: human gut microbes associated with obesity. Nature. 2006; 444(7122):1022-3. DOI: 10.1038/4441022a. View

Dwyer M, Hellinga H . Periplasmic binding proteins: a versatile superfamily for protein engineering. Curr Opin Struct Biol. 2004; 14(4):495-504. DOI: 10.1016/j.sbi.2004.07.004. View

Westover B, Buhler J, Sonnenburg J, Gordon J . Operon prediction without a training set. Bioinformatics. 2004; 21(7):880-8. DOI: 10.1093/bioinformatics/bti123. View

Emsley P, Cowtan K . Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004; 60(Pt 12 Pt 1):2126-32. DOI: 10.1107/S0907444904019158. View

Louis P, Scott K, Duncan S, Flint H . Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol. 2007; 102(5):1197-208. DOI: 10.1111/j.1365-2672.2007.03322.x. View

10.

Martens E, Koropatkin N, Smith T, Gordon J . Complex glycan catabolism by the human gut microbiota: the Bacteroidetes Sus-like paradigm. J Biol Chem. 2009; 284(37):24673-7. PMC: 2757170. DOI: 10.1074/jbc.R109.022848. View

11.

Sonnenburg E, Sonnenburg J, Manchester J, Hansen E, Chiang H, Gordon J . A hybrid two-component system protein of a prominent human gut symbiont couples glycan sensing in vivo to carbohydrate metabolism. Proc Natl Acad Sci U S A. 2006; 103(23):8834-9. PMC: 1472243. DOI: 10.1073/pnas.0603249103. View

12.

Eckburg P, Bik E, Bernstein C, Purdom E, Dethlefsen L, Sargent M . Diversity of the human intestinal microbial flora. Science. 2005; 308(5728):1635-8. PMC: 1395357. DOI: 10.1126/science.1110591. View

13.

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(2):1006-12. PMC: 1392924. DOI: 10.1128/AEM.72.2.1006-1012.2006. View

14.

Koropatkin N, Martens E, Gordon J, Smith T . Starch catabolism by a prominent human gut symbiont is directed by the recognition of amylose helices. Structure. 2008; 16(7):1105-15. PMC: 2563962. DOI: 10.1016/j.str.2008.03.017. View

15.

Roberfroid M, Gibson G, Delzenne N . The biochemistry of oligofructose, a nondigestible fiber: an approach to calculate its caloric value. Nutr Rev. 1993; 51(5):137-46. DOI: 10.1111/j.1753-4887.1993.tb03090.x. View

16.

Koropatkin N, Martens E, Gordon J, Smith T . Structure of a SusD homologue, BT1043, involved in mucin O-glycan utilization in a prominent human gut symbiont. Biochemistry. 2009; 48(7):1532-42. PMC: 2655733. DOI: 10.1021/bi801942a. View

17.

Menne E, Guggenbuhl N, Roberfroid M . Fn-type chicory inulin hydrolysate has a prebiotic effect in humans. J Nutr. 2000; 130(5):1197-9. DOI: 10.1093/jn/130.5.1197. View

18.

Cantarel B, Coutinho P, Rancurel C, Bernard T, Lombard V, Henrissat B . The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2008; 37(Database issue):D233-8. PMC: 2686590. DOI: 10.1093/nar/gkn663. View

19.

Bolam D, Xie H, Pell G, Hogg D, Galbraith G, Henrissat B . X4 modules represent a new family of carbohydrate-binding modules that display novel properties. J Biol Chem. 2004; 279(22):22953-63. DOI: 10.1074/jbc.M313317200. View

20.

Xu J, Mahowald M, Ley R, Lozupone C, Hamady M, Martens E . Evolution of symbiotic bacteria in the distal human intestine. PLoS Biol. 2007; 5(7):e156. PMC: 1892571. DOI: 10.1371/journal.pbio.0050156. View