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Journal Article

Ribosome provisioning activates a bistable switch coupled to fast exit from stationary phase

MPS-Authors
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McConnell,  Ellen
Department Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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De Monte,  Silvia
Research Group Dynamics of Microbial Collectives, Department Evolutionary Theory, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Rogers,  David W.
Department Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Rainey,  Paul B.
Department Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Max Planck Society;

Fulltext (public)

msz041.pdf
(Publisher version), 2MB

Supplementary Material (public)

msz041_supp.pdf
(Supplementary material), 4MB

Citation

Remigi, P., Ferguson, G. C., McConnell, E., De Monte, S., Rogers, D. W., & Rainey, P. B. (2019). Ribosome provisioning activates a bistable switch coupled to fast exit from stationary phase. Molecular Biology and Evolution, 36(5), 1056-1070. doi:10.1093/molbev/msz041.


Cite as: http://hdl.handle.net/21.11116/0000-0003-70B3-4
Abstract
Observations of bacteria at the single-cell level have revealed many instances of phenotypic heterogeneity within otherwise clonal populations, but the selective causes, molecular bases, and broader ecological relevance remain poorly understood. In an earlier experiment in which the bacterium Pseudomonas fluorescens SBW25 was propagated under a selective regime that mimicked the host immune response, a genotype evolved that stochastically switched between capsulation states. The genetic cause was a mutation in carB that decreased the pyrimidine pool (and growth rate), lowering the activation threshold of a preexisting but hitherto unrecognized phenotypic switch. Genetic components surrounding bifurcation of UTP flux toward DNA/RNA or UDP-glucose (a precursor of colanic acid forming the capsules) were implicated as key components. Extending these molecular analyses—and based on a combination of genetics, transcriptomics, biochemistry, and mathematical modeling—we show that pyrimidine limitation triggers an increase in ribosome biosynthesis and that switching is caused by competition between ribosomes and CsrA/RsmA proteins for the mRNA transcript of a positively autoregulated activator of colanic acid biosynthesis. We additionally show that in the ancestral bacterium the switch is part of a program that determines stochastic entry into a semiquiescent capsulated state, ensures that such cells are provisioned with excess ribosomes, and enables provisioned cells to exit rapidly from stationary phase under permissive conditions.