Global physiological analysis of carbon- and energy-limited growing Escherichia coli confirms a high degree of catabolic flexibility and preparedness for mixed substrate utilization

Growth conditions for heterotrophic bacteria in the environment are characterized by low concentrations of carbon and energy sources and complex substrate mixtures. While mechanisms of starvation-survival in the absence of carbon substrates have been studied in considerable detail, information on the physiology of slow growth under oligotrophic conditions is limited. We intended to elucidate general strategies by which Escherichia coli adapts to low concentrations of a mixed carbon and energy source pool. A new screening method based on BIOLOG AN MicroPlates, which allowed us to distinguish repressed and induced catabolic functions in E. coli, was combined with the analysis of periplasmic high-affinity binding proteins. Extending previous findings for E. coli and other microbial species, we found that numerous alternative catabolic functions and high-affinity binding proteins are derepressed under either glucose- or arabinose-limited growth conditions, in spite of the absence of the respective inducers. Escherichia coli cells growing in carbon-limited complex medium chemostat cultures exhibited an even higher degree of catabolic flexibility and were able to oxidize 43 substrates. The BIOLOG respiration pattern indicated simultaneous dissimilation of diverse sugars, amino acids and dipeptides (mixed substrate growth). The observed physiological adaptations of E. coli to low concentrations of carbon and energy substrates presumably are advantageous in many natural growth situations and also offer an explanation why many heterotrophic bacteria have and maintain such a broad carbon substrate range.