Acetate Exposure Determines the Diauxic Behavior of Escherichia coli during the Glucose-Acetate Transition

Abstract

Growth of Escherichia coli on glucose in batch culture is accompanied by the excretion of acetate, which is consumed by the cells when glucose is exhausted. This glucose-acetate transition is classically described as a diauxie (two successive growth stages). Here, we investigated the physiological and metabolic properties of cells after glucose exhaustion through the analysis of growth parameters and gene expression. We found that E. coli cells grown on glucose in batch culture produce acetate and consume it after glucose exhaustion but do not grow on acetate. Acetate is catabolized, but key anabolic genes--such as the genes encoding enzymes of the glyoxylate shunt--are not upregulated, hence preventing growth. Both the induction of the latter anabolic genes and growth were observed only after prolonged exposure to low concentrations of acetate and could be accelerated by high acetate concentrations. We postulate that such decoupling between acetate catabolism and acetate anabolism might be an advantage for the survival of E. coli in the ever-changing environment of the intestine.

Importance: The glucose-acetate transition is a valuable experimental model for comprehensive investigations of metabolic adaptation and a current paradigm for developing modeling approaches in systems microbiology. Yet, the work reported in our paper demonstrates that the metabolic behavior of Escherichia coli during the glucose-acetate transition is much more complex than what has been reported so far. A decoupling between acetate catabolism and acetate anabolism was observed after glucose exhaustion, which has not been reported previously. This phenomenon could represent a strategy for optimal utilization of carbon resources during colonization and persistence of E. coli in the gut and is also of significant interest for biotechnological applications.