A Molecular Sensor That Allows a Gut Commensal to Control Its Nutrient Foundation in a Competitive Ecosystem

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1999 Aug 18

PMID 10449780

Citations 168

Authors

L V Hooper

J Xu

P G Falk

T Midtvedt

J I Gordon

Affiliations

Soon will be listed here.

Abstract

Little is known about how members of the indigenous microflora interact with their mammalian hosts to establish mutually beneficial relationships. We have used a gnotobiotic mouse model to show that Bacteroides thetaiotaomicron, a component of the intestinal microflora of mice and humans, uses a repressor, FucR, as a molecular sensor of L-fucose availability. FucR coordinates expression of an operon encoding enzymes in the L-fucose metabolic pathway with expression of another locus that regulates production of fucosylated glycans in intestinal enterocytes. Genetic and biochemical studies indicate that FucR does this by using fucose as an inducer at one locus and as a corepressor at the other locus. Coordinating this commensal's immediate nutritional requirements with production of a host-derived energy source is consistent with its need to enter and persist within a competitive ecosystem.

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References

Moore W, Holdeman L . Human fecal flora: the normal flora of 20 Japanese-Hawaiians. Appl Microbiol. 1974; 27(5):961-79. PMC: 380185. DOI: 10.1128/am.27.5.961-979.1974. View

Anderson R, Wood W . Purification and properties of L-xylulokinase. J Biol Chem. 1962; 237:1029-33. View

Guiney D, Yakobson E . Location and nucleotide sequence of the transfer origin of the broad host range plasmid RK2. Proc Natl Acad Sci U S A. 1983; 80(12):3595-8. PMC: 394096. DOI: 10.1073/pnas.80.12.3595. View

Ushijima T, Takahashi M, Tatewaki K, Ozaki Y . A selective medium for isolation and presumptive identification of the Bacteriodes fragilis group. Microbiol Immunol. 1983; 27(12):985-93. DOI: 10.1111/j.1348-0421.1983.tb02929.x. View

Bartkus J, Mortlock R . Isolation of a mutation resulting in constitutive synthesis of L-fucose catabolic enzymes. J Bacteriol. 1986; 165(3):710-4. PMC: 214487. DOI: 10.1128/jb.165.3.710-714.1986. View

Shoemaker N, Getty C, GARDNER J, Salyers A . Tn4351 transposes in Bacteroides spp. and mediates the integration of plasmid R751 into the Bacteroides chromosome. J Bacteriol. 1986; 165(3):929-36. PMC: 214518. DOI: 10.1128/jb.165.3.929-936.1986. View

McCarthy R, Salyers A . Evidence that polygalacturonic acid may not be a major source of carbon and energy for some colonic Bacteroides species. Appl Environ Microbiol. 1986; 52(1):9-16. PMC: 203385. DOI: 10.1128/aem.52.1.9-16.1986. View

Brenowitz M, Senear D, Shea M, Ackers G . Quantitative DNase footprint titration: a method for studying protein-DNA interactions. Methods Enzymol. 1986; 130:132-81. DOI: 10.1016/0076-6879(86)30011-9. View

Bjork S, Breimer M, Hansson G, Karlsson K, Leffler H . Structures of blood group glycosphingolipids of human small intestine. A relation between the expression of fucolipids of epithelial cells and the ABO, Le and Se phenotype of the donor. J Biol Chem. 1987; 262(14):6758-65. View

10.

Chen Y, Zhu Y, Lin E . The organization of the fuc regulon specifying L-fucose dissimilation in Escherichia coli K12 as determined by gene cloning. Mol Gen Genet. 1987; 210(2):331-7. DOI: 10.1007/BF00325702. View

11.

Finne J, Breimer M, Hansson G, Karlsson K, Leffler H, Vliegenthart J . Novel polyfucosylated N-linked glycopeptides with blood group A, H, X, and Y determinants from human small intestinal epithelial cells. J Biol Chem. 1989; 264(10):5720-35. View

12.

Lu Z, Lin E . The nucleotide sequence of Escherichia coli genes for L-fucose dissimilation. Nucleic Acids Res. 1989; 17(12):4883-4. PMC: 318048. DOI: 10.1093/nar/17.12.4883. View

13.

Van Der Waaij D . The ecology of the human intestine and its consequences for overgrowth by pathogens such as Clostridium difficile. Annu Rev Microbiol. 1989; 43:69-87. DOI: 10.1146/annurev.mi.43.100189.000441. View

14.

Salyers A, Pajeau M . Competitiveness of different polysaccharide utilization mutants of Bacteroides thetaiotaomicron in the intestinal tracts of germfree mice. Appl Environ Microbiol. 1989; 55(10):2572-8. PMC: 203124. DOI: 10.1128/aem.55.10.2572-2578.1989. View

15.

Brassart D, Woltz A, Golliard M, Neeser J . In vitro inhibition of adhesion of Candida albicans clinical isolates to human buccal epithelial cells by Fuc alpha 1----2Gal beta-bearing complex carbohydrates. Infect Immun. 1991; 59(5):1605-13. PMC: 257891. DOI: 10.1128/iai.59.5.1605-1613.1991. View

16.

Haydon D, Guest J . A new family of bacterial regulatory proteins. FEMS Microbiol Lett. 1991; 63(2-3):291-5. DOI: 10.1016/0378-1097(91)90101-f. View

17.

Tancula E, Feldhaus M, Bedzyk L, Salyers A . Location and characterization of genes involved in binding of starch to the surface of Bacteroides thetaiotaomicron. J Bacteriol. 1992; 174(17):5609-16. PMC: 206506. DOI: 10.1128/jb.174.17.5609-5616.1992. View

18.

Cheng Q, Hwa V, Salyers A . A locus that contributes to colonization of the intestinal tract by Bacteroides thetaiotaomicron contains a single regulatory gene (chuR) that links two polysaccharide utilization pathways. J Bacteriol. 1992; 174(22):7185-93. PMC: 207410. DOI: 10.1128/jb.174.22.7185-7193.1992. View

19.

Sadlack B, Merz H, Schorle H, Schimpl A, Feller A, Horak I . Ulcerative colitis-like disease in mice with a disrupted interleukin-2 gene. Cell. 1993; 75(2):253-61. DOI: 10.1016/0092-8674(93)80067-o. View

20.

Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W . Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 1993; 75(2):263-74. DOI: 10.1016/0092-8674(93)80068-p. View