Glycogen and maltose utilization by Escherichia coli O157:H7 in the mouse intestine - PubMed (original) (raw)

Glycogen and maltose utilization by Escherichia coli O157:H7 in the mouse intestine

Shari A Jones et al. Infect Immun. 2008 Jun.

Abstract

Mutant screens and transcriptome studies led us to consider whether the metabolism of glucose polymers, i.e., maltose, maltodextrin, and glycogen, is important for Escherichia coli colonization of the intestine. By using the streptomycin-treated mouse model, we found that catabolism of the disaccharide maltose provides a competitive advantage in vivo to pathogenic E. coli O157:H7 and commensal E. coli K-12, whereas degradation of exogenous forms of the more complex glucose polymer, maltodextrin, does not. The endogenous glucose polymer, glycogen, appears to play an important role in colonization, since mutants that are unable to synthesize or degrade glycogen have significant colonization defects. In support of the hypothesis that E. coli relies on internal carbon stores to maintain colonization during periods of famine, we found that by providing a constant supply of a readily metabolized sugar, i.e., gluconate, in the animal's drinking water, the competitive disadvantage of E. coli glycogen metabolism mutants is rescued. The results suggest that glycogen storage may be widespread in enteric bacteria because it is necessary for maintaining rapid growth in the intestine, where there is intense competition for resources and occasional famine. An important implication of this study is that the sugars used by E. coli are present in limited quantities in the intestine, making endogenous carbon stores valuable. Thus, there may be merit to combating enteric infections by using probiotics or prebiotics to manipulate the intestinal microbiota in such a way as to limit the availability of sugars preferred by E. coli O157:H7 and perhaps other pathogens.

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Figures

FIG. 1.

FIG. 1.

E. coli EDL933 ppsA pckA malP::mini-Tn_5_-Km2 STM is outcompeted by E. coli EDL933 ppsA pckA during colonization. Strains were fed to mice at 105 CFU each.

FIG. 2.

FIG. 2.

Phenotypes of E. coli EDL933 mutants used in the present study. Growth on maltose or maltodextrin as the sole carbon source was determined in MOPS medium containing 0.2% carbohydrate. Maltose and maltodextrin sensitivity was determined in LB containing 0.2% carbohydrate. The final OD600 values of cultures at 24 h are shown. Oxidation of maltose was determined on Biolog GN2 phenotype plates, as shown in graphlets of relative amounts of substrate oxidized (y axis) versus time. Glycogen accumulation on LB agar containing 2% glucose was visualized by staining with iodine vapor.

FIG. 3.

FIG. 3.

Maltose/maltodextrin transport mutants display colonization defects. (A) E. coli EDL933 Δ(malE-malG) has a colonization defect in competition with E. coli EDL933 wild-type. (B) E. coli EDL933 Δ_malX_ does not exhibit a colonization defect. (C) E. coli EDL933 Δ_malX_ Δ(malE-malG) has a colonization defect in competition with E. coli EDL933 wild-type. (D) E. coli EDL933 Δ_lamB_ does not exhibit a colonization defect. Strains were fed to mice at 105 CFU each.

FIG. 4.

FIG. 4.

Catabolism of maltose but not maltodextrins is important for competitive colonization of the mouse intestine. (A) E. coli EDL933 Δ(malP-malQ) has colonization defect in competition with E. coli EDL933 wild-type. (B) E. coli EDL933 Δ_malQ_ has colonization defect in competition with E. coli EDL933 wild-type. (C) E. coli EDL933 Δ_malP_ does not exhibit a significant colonization defect. Strains were fed to mice at 105 CFU each.

FIG. 5.

FIG. 5.

Catabolism of maltose is necessary for E. coli EDL933 to compete efficiently with wild-type E. coli MG1655 in the mouse intestine. (A) E. coli EDL933 wild-type (fed to mice at 105 CFU) initially out competes higher numbers of E. coli MG1655 wild-type (fed at 1010 CFU). (B) E. coli EDL933 Δ_malQ_ (fed at 105 CFU) cannot compete with higher numbers of E. coli MG1655 wild-type (fed at 1010 CFU).

FIG. 6.

FIG. 6.

Glycogen synthesis mutants do not compete effectively in the mouse intestine. (A) E. coli EDL933 Δ_glgA_ exhibits colonization defect in competition with E. coli EDL933 wild-type. (B) E. coli EDL933 Δ_glgS_ exhibits colonization defect in competition with E. coli EDL933 wild-type. Strains were fed to mice at 105 CFU each.

FIG. 7.

FIG. 7.

Colonization defects of glycogen degradation mutants are rescued by adding 2% gluconate to drinking water of mice. (A) E. coli EDL933 Δ_glgP_ and (C) E. coli MG1655 Δ_glgP_ exhibit colonization defects in competition with their respective wild-type parents. (B and D) These colonization defects are rescued by addition of gluconate to the drinking water . Strains were fed to mice at 105 CFU each.

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