Cited by 99Evolution and Genetic DynamicsBacterial Genetics and BiotechnologyGene Regulatory Network Analysis

Compensatory Evolution of Gene Regulation in Response to Stress by Escherichia coli Lacking RpoS

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Stoebel, Daniel M., Hokamp, Karsten, Last, Michael S., Dorman, Charles J.·2009·PLoS Genetics

Abstract

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.

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  • High mutation rates and mutator strains can emerge naturally during laboratory evolution and contribute to the formation of genetic novelty.

    “Interestingly, it was shown that high mutation rates and mutator strains can emerge naturally during laboratory evolution and contribute to the formation of genetic novelty [33,73,139-141].”
  • At least one evolution experiment showed that the general principles observed for E. coli and S. cerevisiae, including the tendency towards optimized biomass yield and overflow metabolism, large-scale regulatory changes and mutator strains, also emerge in Lactococcus lactis.

    “Although rare at this point, at least one evolution experiment showed that the general principles that were observed for E. coli and S. cerevisiae, including the tendency towards optimized biomass yield and overflow metabolism, large-scale regulatory changes and mutator strains also emerge in other microbial hosts, such as Lactococcus lactis[73].”

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Authors
Stoebel, D. M., Hokamp, K., Last, M. S., & Dorman, C. J.
Affiliations
  • Trinity College Dublin (IE)
  • University of California, Davis (US)
Corresponding author
Dorman, Charles J.
Venue
PLoS Genetics
Published
2009-10-02
Volume
5
Issue
10
Pages
e1000671
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
OpenAlex
W2163316690
Cited by
99
References
55
Citations by year
2026: 2 · 2025: 3 · 2024: 3 · 2023: 6 · 2022: 3 · 2021: 1 · 2020: 7 · 2019: 8 · 2018: 4 · 2017: 14 · 2016: 4 · 2015: 7 · 2014: 6 · 2013: 6 · 2012: 7
FWCI
4.85
Type
journal article
Language
en
Open access
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Scholarship - Claremont (Claremont Colleges) (submittedVersion)
  • Arrow@dit (Dublin Institute of Technology) (submittedVersion, cc-by-nc-sa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • Wellcome Trust (080054/Z/06/Z, 080054)
  • Science Foundation Ireland (07/IN1/B918)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
Keywords
RpoS sigma factor, gene regulatory evolution, osmotic stress, trehalose biosynthesis, transcriptional regulation, adaptive mutation, Escherichia coli, transcriptional regulatory networks, compensatory evolution
MeSH terms
Bacterial Proteins, Escherichia coli, Sigma Factor, Stress, Physiological, Gene Expression Regulation, Bacterial, Evolution, Molecular

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