Evolution combined with genomic study elucidates genetic bases of isobutanol tolerance in Escherichia coli
Open accessAbstract
Background: Isobutanol is a promising next-generation biofuel with demonstrated high yield microbial production, but the toxicity of this molecule reduces fermentation volumetric productivity and final titer. Organic solvent tolerance is a complex, multigenic phenotype that has been recalcitrant to rational engineering approaches. We apply experimental evolution followed by genome resequencing and a gene expression study to elucidate genetic bases of adaptation to exogenous isobutanol stress. Results: The adaptations acquired in our evolved lineages exhibit antagonistic pleiotropy between minimal and rich medium, and appear to be specific to the effects of longer chain alcohols. By examining genotypic adaptation in multiple independent lineages, we find evidence of parallel evolution in marC,hfq,mdh,acrAB, gatYZABCD, and rph genes. Many isobutanol tolerant lineages show reduced RpoS activity, perhaps related to mutations in hfq or acrAB. Consistent with the complex, multigenic nature of solvent tolerance, we observe adaptations in a diversity of cellular processes. Many adaptations appear to involve epistasis between different mutations, implying a rugged fitness landscape for isobutanol tolerance. We observe a trend of evolution targeting post-transcriptional regulation and high centrality nodes of biochemical networks. Collectively, the genotypic adaptations we observe suggest mechanisms of adaptation to isobutanol stress based on remodeling the cell envelope and surprisingly, stress response attenuation. Conclusions: We have discovered a set of genotypic adaptations that confer increased tolerance to exogenous isobutanol stress. Our results are immediately useful to further efforts to engineer more isobutanol tolerant host strains of E. coli for isobutanol production. We suggest that rpoS and post-transcriptional regulators, such as hfq, RNA helicases, and sRNAs may be interesting mutagenesis targets for future global phenotype engineering.
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E. coli can evolve different modes of lacZ expression depending on the environment that contained either lactose, glucose or both as carbon sources.
“Moreover, recent data showed that E. coli can evolve different modes of lacZ expression, depending on the environment that contained either lactose, glucose or both as carbon sources.”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [76]
Mutations that lead to altered lacZ expression patterns accumulated predominantly in lacI and lacO1 regions of the lac operon, and were responsible for a reduced diauxic lag phase and increased maximum growth rates in lactose growth medium.
“Mutations that lead to altered expression patterns accumulated predominantly in lacI and lacO1 regions of the lac operon [76]. Altogether, these mutations were responsible for a reduced (diauxic) lag phase and increased maximum growth rates in lactose growth medium.”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [76]
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Regulatory mechanisms related to biofuel tolerance in producing microbes
Fu, Y., Chen, L., & Zhang, W. (2016) · Journal of Applied Microbiology · doi:10.1111/jam.13162 · Cited by 13 · see citing works
- Authors
- Minty, J. J., Lesnefsky, A. A., Lin, F., Chen, Y., Zaroff, T. A., Veloso, A. B., Xie, B., McConnell, C. A., Ward, R. J., Schwartz, D. R., Rouillard, J.-M., Gao, Y., Gulari, E., & Lin, X. N.
- Affiliations
- University of Michigan (US)
- Tianjin University (CN)
- Virginia Commonwealth University (US)
- MYcroarray (United States) (US)
- Corresponding author
- Lin, Xiaoxia Nina
- Venue
- Microbial Cell Factories
- Published
- 2011-03-25
- Volume
- 10
- Issue
- 1
- Pages
- 18-18
- ISSN
- 1475-2859 (ISSN-L)
- PMC
- PMC3071312
- OpenAlex
- W1993447713
- Cited by
- 185
- References
- 101
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 6 · 2023: 8 · 2022: 2 · 2021: 11 · 2020: 14 · 2019: 11 · 2018: 11 · 2017: 19 · 2016: 16 · 2015: 15 · 2014: 20 · 2013: 19 · 2012: 20
- FWCI
- 8.69
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Microbial Cell Factories (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Deep Blue (University of Michigan) (submittedVersion)
- VCU Scholars Compass (Virginia Commonwealth University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- National Science Foundation (0926926)
- University of Michigan
- University of Oklahoma
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Escherichia coli, experimental evolution, organic solvent tolerance, parallel evolution, antagonistic pleiotropy, RpoS, Hfq, AcrAB efflux pump, post-transcriptional regulation, epistasis, fitness landscape, stress response attenuation, cell envelope remodeling, isobutanol production, biofuels, gene expression
- MeSH terms
- Butanols, Drug Tolerance, Escherichia coli, Genotype, Lipoproteins, Mutation, Phenotype, Gene Expression Regulation, Bacterial, Genome, Bacterial, Sequence Analysis, DNA, Evolution, Molecular, Oligonucleotide Array Sequence Analysis, Membrane Transport Proteins, ATP-Binding Cassette, Sub-Family C Proteins, Escherichia coli Proteins
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