Reciprocal regulation of L-arabinose and D-xylose metabolism in Escherichia coli

Abstract

Glucose is known to inhibit the transport and metabolism of many sugars in Escherichia coli. This mechanism leads to its preferential consumption. Far less is known about the preferential utilization of nonglucose sugars in E. coli. Two exceptions are L-arabinose and D-xylose. Previous studies have shown that L-arabinose inhibits D-xylose metabolism in Escherichia coli. This repression results from L-arabinose-bound AraC binding to the promoter of the D-xylose metabolic genes and inhibiting their expression. This mechanism, however, has not been explored in single cells. Both the L-arabinose and D-xylose utilization systems are known to exhibit a bimodal induction response to their cognate sugar, where mixed populations of cells either expressing the metabolic genes or not are observed at intermediate sugar concentrations. This suggests that L-arabinose can only inhibit D-xylose metabolism in L-arabinose-induced cells. To understand how cross talk between these systems affects their response, we investigated E. coli during growth on mixtures of L-arabinose and D-xylose at single-cell resolution. Our results showed that mixed, multimodal populations of L-arabinose- and D-xylose-induced cells occurred at intermediate sugar concentrations. We also found that D-xylose inhibited the expression of the L-arabinose metabolic genes and that this repression was due to XylR. These results demonstrate that a strict hierarchy does not exist between L-arabinose and D-xylose as previously thought. The results may also aid in the design of E. coli strains capable of simultaneous sugar consumption.