Single-cell characterization of metabolic switching in the sugar phosphotransferase system of Escherichia coli

Sonja A. Westermayer, Georg Fritz, Joaquín Gutiérrez, Judith A. Megerle, Mira P.S. Weißl, Karin Schnetz, Ulrich Gerland, Joachim O. Rädler

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7 Citations (Scopus)

Abstract

The utilization of several sugars in Escherichia coli is regulated by the Phosphotransferase System (PTS), in which diverse sugar utilization modules compete for phosphoryl flux from the general PTS proteins. Existing theoretical work predicts a winner-take-all outcome when this flux limits carbon uptake. To date, no experimental work has interrogated competing PTS uptake modules with single-cell resolution. Using time-lapse microscopy in perfused microchannels, we analyzed the competition between N-acetyl-glucosamine and sorbitol, as representative PTS sugars, by measuring both the expression of their utilization systems and the concomitant impact of sugar utilization on growth rates. We find two distinct regimes: hierarchical usage of the carbohydrates, and co-expression of the genes for both systems. Simulations of a mathematical model incorporating asymmetric sugar quality reproduce our metabolic phase diagram, indicating that under conditions of nonlimiting phosphate flux, co-expression is due to uncoupling of both sugar utilization systems. Our model reproduces hierarchical winner-take-all behaviour and stochastic co-expression, and predicts the switching between both strategies as a function of available phosphate flux. Hence, experiments and theory both suggest that PTS sugar utilization involves not only switching between the sugars utilized but also switching of utilization strategies to accommodate prevailing environmental conditions.

Original languageEnglish
Pages (from-to)472-485
Number of pages14
JournalMolecular Microbiology
Volume100
Issue number3
DOIs
Publication statusPublished - May 2016
Externally publishedYes

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    Westermayer, S. A., Fritz, G., Gutiérrez, J., Megerle, J. A., Weißl, M. P. S., Schnetz, K., Gerland, U., & Rädler, J. O. (2016). Single-cell characterization of metabolic switching in the sugar phosphotransferase system of Escherichia coli. Molecular Microbiology, 100(3), 472-485. https://doi.org/10.1111/mmi.13329