Carbon nutrition of Escherichia coli in the mouse intestine - PubMed (original) (raw)

Carbon nutrition of Escherichia coli in the mouse intestine

Dong-Eun Chang et al. Proc Natl Acad Sci U S A. 2004.

Abstract

Whole-genome expression profiling revealed Escherichia coli MG1655 genes induced by growth on mucus, conditions designed to mimic nutrient availability in the mammalian intestine. Most were nutritional genes corresponding to catabolic pathways for nutrients found in mucus. We knocked out several pathways and tested the relative fitness of the mutants for colonization of the mouse intestine in competition with their wild-type parent. We found that only mutations in sugar pathways affected colonization, not phospholipid and amino acid catabolism, not gluconeogenesis, not the tricarboxylic acid cycle, and not the pentose phosphate pathway. Gluconate appeared to be a major carbon source used by E. coli MG1655 to colonize, having an impact on both the initiation and maintenance stages. N-acetylglucosamine and N-acetylneuraminic acid appeared to be involved in initiation, but not maintenance. Glucuronate, mannose, fucose, and ribose appeared to be involved in maintenance, but not initiation. The in vitro order of preference for these seven sugars paralleled the relative impact of the corresponding metabolic lesions on colonization: gluconate > N-acetylglucosamine > N-acetylneuraminic acid = glucuronate > mannose > fucose > ribose. The results of this systematic analysis of nutrients used by E. coli MG1655 to colonize the mouse intestine are intriguing in light of the nutrient-niche hypothesis, which states that the ecological niches within the intestine are defined by nutrient availability. Because humans are presumably colonized with different commensal strains, differences in nutrient availability may provide an open niche for infecting E. coli pathogens in some individuals and a barrier to infection in others.

PubMed Disclaimer

Figures

Fig. 1.

Fig. 1.

Expression profiles of E. coli MG1655 genes involved in catabolism of carbohydrates found in mucus (15). Genes are represented in rows, as indicated to the right, and are grouped by the corresponding sugar degradation pathway. PH1, ratio of early logarithmic phase (OD600 = 0.1) cells grown on 10 mg/ml mucus vs. minimal glucose (0.2%); PH2, from the same culture grown to late logarithmic phase (OD600 = 0.3); Low, ratio of cells grown to late logarithmic phase (OD600 = 0.3) on 5 mg/ml mucus vs. minimal glucose; Cont, ratio of cells grown to late logarithmic phase on chemically defined rich medium (20) vs. minimal glucose. Ratios are displayed colorimetrically: bright red indicates genes with ≥2.5-fold higher expression (≈2 standard deviations) and bright green indicates ≤2.5-fold lower expression in the experimental condition compared with minimal glucose; the colors darken to black to indicate no change in expression. GlcNAc, _N-_acetylglucosamine; GalNAc, N- acetylgalactosamine; NANA, sialic acid (_N_-acetylneuraminic acid); GlcNH4, glucosamine. See text for further details.

Fig. 2.

Fig. 2.

Colonization of the mouse intestine by E. coli MG1655 StrR NalR (wild-type) and mutant derivatives of E. coli MG1655 StrR, as follows. Sets of three mice were fed one of the following: 105 cfu each of wild-type and MG1655 StrR Δ_edd_::KmR (KmR, kanamycin-resistant) (A); 105 cfu each of wild-type and MG1655 StrR Δ_manXYZ_::KmR Δ_nagE_ (B); 105 cfu each of wild-type and MG1655 StrR Δ_nanAT_::KmR (C); 105 cfu each of wild-type and MG1655 StrR Δ_fucK_::KmR (D); or 105 cfu each of wild-type and MG1655 StrR Δ_ppsA_ Δ_pckA_::Cm (E). At the indicated times, fecal samples were homogenized, diluted, and plated as described (13). Bars represent standard error of the log10(mean cfu/g of feces) for each set of three mice.

References

    1. Finegold, S. M., Sutter, V. L. & Mathisen, G. E. (1983) in Human Intestinal Microflora in Health and Disease, ed. Hentges, D. J. (Academic, New York), pp. 3-31.
    1. Relman, D. A. & Falkow, S. (2001) Trends Microbiol. 9**,** 206-208. - PubMed
    1. Borrelio, S. P. (1986) in Microbial Metabolism in the Digestive Tract, ed. Hill, M. J. (CRC, Boca Raton, FL), pp. 2-16.
    1. Bryant, M. P. (1974) Am. J. Clin. Nutr. 27**,** 1313-1319. - PubMed
    1. Hill, M. J. (1995) in Role of Gut Bacteria in Human Toxicology and Pharmacology, ed. Hill, M. J. (Taylor and Francis, London), pp. 3-18.

Publication types

MeSH terms

Substances

LinkOut - more resources