l-Fucose Stimulates Utilization ofd-Ribose byEscherichia coliMG1655 ΔfucAOandE. coliNissle 1917 ΔfucAOMutants in the Mouse Intestine and in M9 Minimal Medium

Abstract

Escherichia coli MG1655 uses several sugars for growth in the mouse intestine. To determine the roles of L-fucose and D-ribose, an E. coli MG1655 ⌬fucAO mutant and an E. coli MG1655 ⌬rbsK mutant were fed separately to mice along with wild-type E. coli MG1655. The E. coli MG1655 ⌬fucAO mutant colonized the intestine at a level 2 orders of magnitude lower than that of the wild type, but the E. coli MG1655 ⌬rbsK mutant and the wild type colonized at nearly identical levels. Surprisingly, an E. coli MG1655 ⌬fucAO ⌬rbsK mutant was eliminated from the intestine by either wild-type E. coli MG1655 or E. coli MG1655 ⌬fucAO, suggesting that the ⌬fucAO mutant switches to ribose in vivo. Indeed, in vitro growth experiments showed that L-fucose stimulated utilization of D-ribose by the E. coli MG1655 ⌬fucAO mutant but not by an E. coli MG1655 ⌬fucK mutant. Since the ⌬fucK mutant cannot convert L-fuculose to L-fuculose-1-phosphate, whereas the ⌬fucAO mutant accumulates L-fuculose-1-phosphate, the data suggest that L-fuculose-1-phosphate stimulates growth on ribose both in the intestine and in vitro. An E. coli Nissle 1917 ⌬fucAO mutant, derived from a human probiotic commensal strain, acted in a manner identical to that of E. coli MG1655 ⌬fucAO in vivo and in vitro. Furthermore, L-fucose at a concentration too low to support growth stimulated the utilization of ribose by the wild-type E. coli strains in vitro. Collectively, the data suggest that L-fuculose-1-phosphate plays a role in the regulation of ribose usage as a carbon source by E. coli MG1655 and E. coli Nissle 1917 in the mouse intestine.

Comparison of Carbon Nutrition for Pathogenic and Commensal Escherichia coli Strains in the Mouse Intestine

“…3). The commensal E. coli MG1655, on the other hand, did not respond additively to multiple catabolic lesions, but rather, the catabolic mutant series behaved as if the sequential loss of particular catabolic pathways led to metabolic switches such as the one we recently described for fucose-dependent stimulation of ribose catabolism (2). Perhaps the relative importance of fucose utilization by both E. coli strains in vivo, despite being a low priority substrate in vitro, relates to this presumed "signaling" role of fucose.…”

“…The streptomycin-treated mouse is the model of choice for studying bacterial carbon nutrition in the intestine (7,8,29). We have described this model in considerable detail previously (2,26). We want only to stress here that the streptomycintreated CD-1 mouse is used to study the competition for colonization between two strains, typically a mutant and its wildtype parent; it is not a model for pathogenesis, and none of the animals used in this study showed symptoms of disease at any time during the experiments.…”

Genotype and Phenotypes of an Intestine-Adapted Escherichia coli K-12 Mutant Selected by Animal Passage for Superior Colonization

“…To address the possibility that differences in its transcriptome cause E. coli MG1655* to grow faster on several sugars, we evaluated the expression levels of carbon catabolism gene systems by comparison to the wild-type parent strain, when grown on glucose minimal medium. We focused on 23 carbohydrates that were previously tested for their ability to support intestinal colonization (1,7,15,29) or showed more rapid growth of E. coli MG1655* in vitro (31). The transcriptional network database, RegulonDB, was used to define genes within the corresponding 23 catabolic regulons (52).…”

“…Colonization of the GI tract requires bacteria to effectively compete for these nutrients and maintain a growth rate at least equal to the 2-h turnover rate of the intestinal contents (9)(10)(11). We have shown that of the many traits that possibly make E. coli such a remarkably successful intestinal colonizer, competition for carbon sources plays an important role (1,7,15,29).…”

Discriminating tastes

“…25 Specifically, we found that Spot 42 represses the expression of transporters and catabolic enzymes associated with N-acetylneuraminic acid and L-fucose, while Autieri and coworkers showed that D-ribose consumption requires the L-fucose catabolic genes also targeted by Spot 42. 26 Since consumption of the remaining carbon sources also may be influenced by Spot 42 expression, this sRNA may be an important regulator in enteric bacteria inhabiting the gut.…”