Compensatory evolution of gene regulation in response to stress by Escherichia coli lacking RpoS

The RpoS sigma factor protein of Escherichia coli RNA polymerase is the master transcriptional regulator of physiological responses to a variety of stresses. This stress response comes at the expense of scavenging for scarce resources, causing a trade-off between stress tolerance and nutrient acquis...

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Bibliographic Details
Published in:PLoS genetics 2009-10, Vol.5 (10), p.e1000671-e1000671
Main Authors: Stoebel, Daniel M, Hokamp, Karsten, Last, Michael S, Dorman, Charles J
Format: Article
Language:English
Subjects:
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
E coli
Escherichia coli
Escherichia coli - genetics
Escherichia coli - physiology
Evolution, Molecular
Evolutionary Biology
Experiments
Gene expression
Gene Expression Regulation, Bacterial
Genetic aspects
Genetic regulation
Genetics and Genomics/Gene Expression
Genetics and Genomics/Microbial Evolution and Genomics
Genomes
Hypotheses
Microbiology
Microbiology/Microbial Evolution and Genomics
Mutation
Physiological aspects
Proteins
RNA polymerases
Sigma Factor - genetics
Sigma Factor - metabolism
Stress
Stress, Physiological
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Summary:The RpoS sigma factor protein of Escherichia coli RNA polymerase is the master transcriptional regulator of physiological responses to a variety of stresses. This stress response comes at the expense of scavenging for scarce resources, causing a trade-off between stress tolerance and nutrient acquisition. This trade-off favors non-functional rpoS alleles in nutrient-poor environments. We used experimental evolution to explore how natural selection modifies the regulatory network of strains lacking RpoS when they evolve in an osmotically stressful environment. We found that strains lacking RpoS adapt less variably, in terms of both fitness increase and changes in patterns of transcription, than strains with functional RpoS. This phenotypic uniformity was caused by the same adaptive mutation in every independent population: the insertion of IS10 into the promoter of the otsBA operon. OtsA and OtsB are required to synthesize the osmoprotectant trehalose, and transcription of otsBA requires RpoS in the wild-type genetic background. The evolved IS10 insertion rewires expression of otsBA from RpoS-dependent to RpoS-independent, allowing for partial restoration of wild-type response to osmotic stress. Our results show that the regulatory networks of bacteria can evolve new structures in ways that are both rapid and repeatable.
ISSN:1553-7404
1553-7390
1553-7404
DOI:10.1371/journal.pgen.1000671