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

Loles Hoogerland, Stefan Pieter Hendrik Berg, Yixing Suo, Yuta W. Moriuchi, Adja Zoumaro-Djayoon, Esther Geurken, Flora Yang, Frank Bruggeman, Michael D. Burkart and Gregory Bokinsky ()
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Loles Hoogerland: Delft University of Technology
Stefan Pieter Hendrik Berg: Delft University of Technology
Yixing Suo: University of California
Yuta W. Moriuchi: University of California
Adja Zoumaro-Djayoon: Delft University of Technology
Esther Geurken: Delft University of Technology
Flora Yang: Delft University of Technology
Frank Bruggeman: Vrije Universiteit Amsterdam
Michael D. Burkart: University of California
Gregory Bokinsky: Delft University of Technology

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: Abstract All free-living microorganisms homeostatically maintain the fluidity of their membranes by adapting lipid composition to environmental temperatures. Here, we quantify enzymes and metabolic intermediates of the Escherichia coli fatty acid and phospholipid synthesis pathways, to describe how this organism measures temperature and restores optimal membrane fluidity within a single generation after a temperature shock. A first element of this regulatory system is a temperature-sensitive metabolic valve that allocates flux between the saturated and unsaturated fatty acid synthesis pathways via the branchpoint enzymes FabI and FabB. A 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 strategy 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 mathematical model, which we use to show how hard-wired parameters calibrate the system to generate membrane compositions that maintain constant fluidity across temperatures. We hypothesize that core features of the E. coli system will prove to be ubiquitous features of homeoviscous adaptation systems.

Date: 2024
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DOI: 10.1038/s41467-024-53677-5

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