Competitive Fitness During Feast and Famine: How SOS DNA Polymerases Influence Physiology and Evolution in Escherichia coli
Open accessAbstract
Escherichia coli DNA polymerases (Pol) II, IV, and V serve dual roles by facilitating efficient translesion DNA synthesis while simultaneously introducing genetic variation that can promote adaptive evolution. Here we show that these alternative polymerases are induced as cells transition from exponential to long-term stationary-phase growth in the absence of induction of the SOS regulon by external agents that damage DNA. By monitoring the relative fitness of isogenic mutant strains expressing only one alternative polymerase over time, spanning hours to weeks, we establish distinct growth phase-dependent hierarchies of polymerase mutant strain competitiveness. Pol II confers a significant physiological advantage by facilitating efficient replication and creating genetic diversity during periods of rapid growth. Pol IV and Pol V make the largest contributions to evolutionary fitness during long-term stationary phase. Consistent with their roles providing both a physiological and an adaptive advantage during stationary phase, the expression patterns of all three SOS polymerases change during the transition from log phase to long-term stationary phase. Compared to the alternative polymerases, Pol III transcription dominates during mid-exponential phase; however, its abundance decreases to <20% during long-term stationary phase. Pol IV transcription dominates as cells transition out of exponential phase into stationary phase and a burst of Pol V transcription is observed as cells transition from death phase to long-term stationary phase. These changes in alternative DNA polymerase transcription occur in the absence of SOS induction by exogenous agents and indicate that cell populations require appropriate expression of all three alternative DNA polymerases during exponential, stationary, and long-term stationary phases to attain optimal fitness and undergo adaptive evolution.
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Mutations in carbon source metabolism-associated genes such as lacZ can occur after plating due to adaptive mutagenesis, because the selective agent does not immediately kill the non-mutant cells.
“Mutations in carbon source metabolism-associated genes such as lacZ can occur after plating due to adaptive mutagenesis, because the selective agent does not immediately kill the non-mutant cells [18,19].”
From Efficient, robust, and versatile fluctuation data analysis using MLE MUtation Rate calculator (mlemur) (2023) · cites this paper as [19]
The Discussion (page not available) says Pol IV helps generate mutations in the lac system, supporting the general connection to lactose-related genes. It does not say that lacZ mutations occur after plating or explain them by a selective agent failing to kill non-mutant cells immediately. (LLM, conf=0.81)
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References 73 · Cited by 44
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- Authors
- Corzett, C. H., Goodman, M. F., & Finkel, S. E.
- Affiliations
- University of Southern California (US)
- Corresponding author
- Finkel, Steven E
- Venue
- Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-06-01
- Volume
- 194
- Issue
- 2
- Pages
- 409-420
- ISSN
- 0016-6731 (ISSN-L)
- 1943-2631
- PMC
- PMC3664851
- OpenAlex
- W2158061773
- Cited by
- 44
- References
- 73
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 1 · 2023: 3 · 2022: 3 · 2021: 3 · 2020: 4 · 2019: 1 · 2018: 5 · 2017: 4 · 2016: 8 · 2015: 5 · 2014: 3 · 2013: 1
- FWCI
- 3.76
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Genetics (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (0237975, CAREER)
- National Institutes of Health (GM21422)
- U.S. Air Force
- National Institute of General Medical Sciences (T32GM067587, GM 21422, R37GM021422, T32GM67587, R01GM021422)
- National Institute of Environmental Health Sciences (ES012259, R01ES012259)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Keywords
- DNA polymerase II, DNA polymerase IV, DNA polymerase V, Escherichia coli, stationary phase, exponential growth phase, relative fitness, adaptive evolution, translesion synthesis, DNA replication
- MeSH terms
- Adaptation, Physiological, DNA-Directed DNA Polymerase, Escherichia coli, Mutation, SOS Response, Genetics, Transcription, Genetic, Evolution, Molecular, Escherichia coli Proteins, Cell Proliferation, Genetic Fitness
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