Divergence Involving Global Regulatory Gene Mutations in an Escherichia coli Population Evolving under Phosphate Limitation
Open accessAbstract
Many of the important changes in evolution are regulatory in nature. Sequenced bacterial genomes point to flexibility in regulatory circuits but we do not know how regulation is remodeled in evolving bacteria. Here, we study the regulatory changes that emerge in populations evolving under controlled conditions during experimental evolution of Escherichia coli in a phosphate-limited chemostat culture. Genomes were sequenced from five clones with different combinations of phenotypic properties that coexisted in a population after 37 days. Each of the distinct isolates contained a different mutation in 1 of 3 highly pleiotropic regulatory genes (hfq, spoT, or rpoS). The mutations resulted in dissimilar proteomic changes, consistent with the documented effects of hfq, spoT, and rpoS mutations. The different mutations do share a common benefit, however, in that the mutations each redirect cellular resources away from stress responses that are redundant in a constant selection environment. The hfq mutation lowers several individual stress responses as well the small RNA-dependent activation of rpoS translation and hence general stress resistance. The spoT mutation reduces ppGpp levels, decreasing the stringent response as well as rpoS expression. The mutations in and upstream of rpoS resulted in partial or complete loss of general stress resistance. Our observations suggest that the degeneracy at the core of bacterial stress regulation provides alternative solutions to a common evolutionary challenge. These results can explain phenotypic divergence in a constant environment and also how evolutionary jumps and adaptive radiations involve altered gene regulation.
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Mutational robustness can have a positive effect on evolvability, depending on the population size and network architecture.
“Although counterintuitive at first, it was shown that mutational robustness can have a positive effect on evolvability, depending on the population size and network architecture [41,136].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [41]
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- Authors
- Wang, L., Spira, B., Zhou, Z., Feng, L., Maharjan, R. P., Li, X., Li, F., McKenzie, C., Reeves, P. R., & Ferenci, T.
- Affiliations
- Nankai University (CN)
- The University of Sydney (AU)
- Corresponding author
- Ferenci, Thomas
- ORCID
- Venue
- Genome Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-01-01
- Volume
- 2
- Pages
- 478-487
- ISSN
- 1759-6653 (ISSN-L)
- PMC
- PMC2997555
- OpenAlex
- W2074203599
- Cited by
- 114
- References
- 51
- Citations by year
- 2024: 24 · 2023: 1 · 2022: 2 · 2021: 10 · 2020: 2 · 2019: 3 · 2018: 7 · 2017: 10 · 2016: 4 · 2015: 10 · 2014: 12 · 2013: 8 · 2012: 11
- FWCI
- 5.22
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by-nc
- Locations
- Genome Biology and Evolution (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Scientific Electronic Library Online (São Paulo Research Foundation, Latin American and Caribbean Center on Health Sciences Information, Conselho Nacional de Desenvolvimento Científico e Tecnológico) (publishedVersion)
- Funders
- Fundação de Amparo à Pesquisa do Estado de São Paulo
- National Natural Science Foundation of China (30870070, 973 Program, 863 Program, 30870078, 30771175, 30530010)
- National High-tech Research and Development Program
- National Key Research and Development Program of China
- National Science Fund for Distinguished Young Scholars (30788001)
- National Institute on Alcohol Abuse and Alcoholism (R01AA020703)
- 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 › Genomics and Phylogenetic Studies
- Keywords
- Escherichia coli, phosphate limitation, experimental evolution, Hfq, SPOT, RpoS, stringent response, ppGpp, small RNA, stress response, phenotypic divergence, pleiotropy, chemostat culture, proteomics, adaptive radiation
- MeSH terms
- Bacterial Proteins, Escherichia coli, Genes, Bacterial, Guanosine Tetraphosphate, Models, Genetic, Mutation, Phenotype, Phosphates, Pyrophosphatases, Sigma Factor, Stress, Physiological, Directed Molecular Evolution, Proteome, Escherichia coli Proteins, Host Factor 1 Protein
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