A universal trade-off between growth and lag in fluctuating environments

Markus Basan (), Tomoya Honda, Dimitris Christodoulou, Manuel Hörl, Yu-Fang Chang, Emanuele Leoncini, Avik Mukherjee, Hiroyuki Okano, Brian R. Taylor, Josh M. Silverman, Carlos Sanchez, James R. Williamson, Johan Paulsson, Terence Hwa () and Uwe Sauer ()
Additional contact information
Markus Basan: Harvard Medical School
Tomoya Honda: University of California at San Diego
Dimitris Christodoulou: ETH Zürich
Manuel Hörl: ETH Zürich
Yu-Fang Chang: Harvard Medical School
Emanuele Leoncini: Harvard Medical School
Avik Mukherjee: Harvard Medical School
Hiroyuki Okano: University of California at San Diego
Brian R. Taylor: University of California at San Diego
Josh M. Silverman: The Scripps Research Institute
Carlos Sanchez: Harvard Medical School
James R. Williamson: The Scripps Research Institute
Johan Paulsson: Harvard Medical School
Terence Hwa: University of California at San Diego
Uwe Sauer: ETH Zürich

Nature, 2020, vol. 584, issue 7821, 470-474

Abstract: Abstract The rate of cell growth is crucial for bacterial fitness and drives the allocation of bacterial resources, affecting, for example, the expression levels of proteins dedicated to metabolism and biosynthesis1,2. It is unclear, however, what ultimately determines growth rates in different environmental conditions. Moreover, increasing evidence suggests that other objectives are also important3–7, such as the rate of physiological adaptation to changing environments8,9. A common challenge for cells is that these objectives cannot be independently optimized, and maximizing one often reduces another. Many such trade-offs have indeed been hypothesized on the basis of qualitative correlative studies8–11. Here we report a trade-off between steady-state growth rate and physiological adaptability in Escherichia coli, observed when a growing culture is abruptly shifted from a preferred carbon source such as glucose to fermentation products such as acetate. These metabolic transitions, common for enteric bacteria, are often accompanied by multi-hour lags before growth resumes. Metabolomic analysis reveals that long lags result from the depletion of key metabolites that follows the sudden reversal in the central carbon flux owing to the imposed nutrient shifts. A model of sequential flux limitation not only explains the observed trade-off between growth and adaptability, but also allows quantitative predictions regarding the universal occurrence of such tradeoffs, based on the opposing enzyme requirements of glycolysis versus gluconeogenesis. We validate these predictions experimentally for many different nutrient shifts in E. coli, as well as for other respiro-fermentative microorganisms, including Bacillus subtilis and Saccharomyces cerevisiae.

Date: 2020
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DOI: 10.1038/s41586-020-2505-4

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