A temperature-sensitive metabolic valve and a transcriptional feedback loop drive rapid homeoviscous adaptation in Escherichia coli

Abstract

All free-living microorganisms homeostatically maintain the fluidity of their membranes by adapting lipid composition to environmental temperatures. A quantitative description of how organisms maintain constant fluidity at all growth temperatures has not been achieved. By quantifying both enzymes and metabolic intermediates of the Escherichia coli fatty acid and phospholipid synthesis pathways, we discover how E. coli measures steady-state temperature and restores optimal membrane fluidity within a single generation after temperature shocks. The first element of the system is a temperature-sensitive metabolic valve that allocates flux between the saturated and unsaturated fatty acid synthesis pathways. The second element is a transcription-based negative feedback loop that counteracts the temperature-sensitive valve. The combination of these elements accelerates membrane adaptation by causing a transient overshoot in the synthesis of saturated or unsaturated fatty acids following temperature shocks. This overshoot strategy accelerates membrane adaptation, and is comparable to increasing the temperature of a water bath by adding water that is excessively hot rather than adding water at the desired temperature. These properties are captured in a quantitative model, which we further use to show how hard-wired parameters calibrate the system to generate membrane compositions that maintain constant fluidity across a wide range of temperatures. We hypothesize that core design features of the E. coli system will prove to be ubiquitous features of homeoviscous adaptation systems.