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Adaptive Evolution of Escherichia coli K-12 MG1655 during Growth on a Nonnative Carbon Source,l-1,2-Propanediol
Open accessAbstract
Laboratory adaptive evolution studies can provide key information to address a wide range of issues in evolutionary biology. Such studies have been limited thus far by the inability of workers to readily detect mutations in evolved microbial strains on a genome scale. This limitation has now been overcome by recently developed genome sequencing technology that allows workers to identify all accumulated mutations that appear during laboratory adaptive evolution. In this study, we evolved Escherichia coli K-12 MG1655 with a nonnative carbon source,l-1,2-propanediol (l-1,2-PDO), for ∼700 generations. We found that (i) experimental evolution of E. coli for ∼700 generations in 1,2-PDO-supplemented minimal medium resulted in acquisition of the ability to use l-1,2-PDO as a sole carbon and energy source so that the organism changed from an organism that did not grow at all initially to an organism that had a growth rate of 0.35 h−1; (ii) six mutations detected by whole-genome resequencing accumulated in the evolved E. coli mutant over the course of adaptive evolution on l-1,2-PDO; (iii) five of the six mutations were within coding regions, and IS 5 was inserted between two fuc regulons; (iv) two major mutations (mutations in fucO and its promoter) involved in l-1,2-PDO catabolism appeared early during adaptive evolution; and (v) multiple defined knock-in mutant strains with all of the mutations had growth rates essentially matching that of the evolved strain. These results provide insight into the genetic basis underlying microbial evolution for growth on a nonnative substrate.
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“Whereas certain environments can lead to fast selection of improved phenotypes, others, including the long-term adaptation to environmental pH [59,63], represent complex environments where microbial cells show low adaptive potential in terms of absolute fitness gain.”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [63]
In the citing paper
“In several recent studies, gene amplifications were identified to contribute to increased gene dosage [63,116,128] and subsequently increased fitness.”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [63]
In the citing paper
“Frequent rpoB mutations were also found during batch evolution on glucose in a more recent study [63]”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [63]
In the citing paper
“Increased growth during osmotic stress was linked to mutations that led to increased expression of enterobactin biosynthesis genes (fepA and entD among others) [63].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [63]
In the citing paper
“but most importantly the rpoS mutation alone did not positively influence the growth rate in the ancestral ∆pgi strain; rpoS mutations were epistatically linked to additional mutations.”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [63]
In the citing paper
“Mutations in acrAB and marC were found independently in these studies; further changes were linked to carbon and nitrogen metabolism via gatY and tnaA[86], enterobactin synthesis [63] or attenuated rpoS activity via hfq mutations [87].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [63]
In the citing paper
“and n-butanol tolerance is weakly compatible with oxidative stress [63] and leads to trade-offs in hexane and chloramphenicol resistance [86].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [63]
In the citing paper
“Similarly, n-butanol tolerance was reported to be highly compatible with osmotic stress [63].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [63]
In the citing paper
“Furthermore, increased oxidative stress resistance in E. coli may be linked to mutations in the soxR reducing system and increased levels of cellular catalase/peroxidase (katG) [63].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [63]
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“The optimization of genomes can also be performed by experimental evolution, selecting for favorable genotypes [49,50].”
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“Whereas experiments probing adaptive genetic changes of wild-type bacterial cells to a range of growth and stress conditions are prevalent [5-14], studies investigating adaptive evolutionary trajectories from different genetic starting states are less common [15-18].”
BackgroundZhang, B., Li, N., Wang, Z., Ya-jie Tang, A., Chen, T., & Zhao, X. (2014) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-014-6131-7 · Cited by 35
Genomic analysis of parallel-evolved cyanobacterium Synechocystis sp. PCC 6803 under acid stress
Uchiyama, J., Kanesaki, Y., Iwata, N., Asakura, R., Funamizu, K., Tasaki, R., Agatsuma, M., Tahara, H., Matsuhashi, A., Yoshikawa, H., et al. (2015) · Photosynthesis Research · doi:10.1007/s11120-015-0111-3 · Cited by 34
“Pseudomonas aeruginosa, and Saccharomyces cerevisiae (Lee and Palsson 2010; Dettman et al. 2012; Oud et al. 2012; Wong et al. 2012).”
The role of cellular objectives and selective pressures in metabolic pathway evolution
Nam, H., Conrad, T. M., & Lewis, N. E. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.03.006 · Cited by 32
“It evolved the ability to metabolize L-1,2-PDO when glycerol minimal media was slowly replaced with L-1,2-PDO minimal media [24].”
Promoter propagation in prokaryotes
Matus, M. G., Nijveen, H., & van Passel, M. W. J. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks787 · Cited by 33
Accelerated adaptive laboratory evolution: A tool for evolutionary biotechnology
Declerck, L., Bouchon, F., Demeester, W., Guidi, C., & Mey, M. D. (2025) · Biotechnology Advances · doi:10.1016/j.biotechadv.2025.108741 · Cited by 32
Effect of long-term laboratory propagation on Chlamydia trachomatis genome dynamics
Borges, V., Ferreira, R., Nunes, A., Sousa‐Uva, M., Abreu, M., Borrego, M. J., & Gomes, J. P. (2013) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2013.03.035 · Cited by 30
Setting the stage for evolution of a new enzyme
Copley, S. D. (2021) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2021.03.001 · Cited by 28
Trait drift in microalgae and applications for strain improvement
Jebali, A., Sanchez, M. R., Hanschen, E. R., Starkenburg, S. R., & Corcoran, A. A. (2022) · Biotechnology Advances · doi:10.1016/j.biotechadv.2022.108034 · Cited by 30
Graf, M., Haas, T., Müller, F., Buchmann, A., Harm-Bekbenbetova, J., Freund, A., Nieß, A., Persicke, M., Kalinowski, J., Blombach, B., et al. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01648 · Cited by 27
Kim, H. J., Turner, T. L., & Jin, Y. (2013) · Biotechnology Advances · doi:10.1016/j.biotechadv.2013.03.010 · Cited by 29
Evolutionary history and genetic parallelism affect correlated responses to evolution
Gac, M. L., Cooper, T. F., Cruveiller, S., Médigue, C., & Schneider, D. (2013) · Molecular Ecology · doi:10.1111/mec.12312 · Cited by 28
“…in genes specifically involved in the catabolic pathways of the available carbon sources in populations propagated in the presence of glycerol (Herring et al. 2006) and L-1,2-propanediol (Lee & Palsson 2010), but not in the presence of lactate (Conrad et al. 2009) or glucose (Barrick et al. 2009).”
BackgroundEvolutionary Consequence of a Trade-Off between Growth and Maintenance along with Ribosomal Damages
Ying, B., Honda, T., Tsuru, S., Seno, S., Matsuda, H., Kazuta, Y., & Yomo, T. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135639 · Cited by 26
Zheng, Y., Kong, S., Luo, S., Chen, C., Cui, Z., Sun, X. H., Chen, T., & Wang, Z. (2022) · ACS Sustainable Chemistry & Engineering · doi:10.1021/acssuschemeng.1c05783 · Cited by 28
Dispensability of Escherichia coli ’s latent pathways
Cornelius, S. P., Lee, J. S., & Motter, A. E. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1009772108 · Cited by 26
“If the perturbation is nonlethal, the perturbed organisms will undergo adaptive evolution—adopting beneficial mutations over longer timescales (23, 24) to achieve a new optimal growth state, which can be predicted by FBA (18, 25).”
BackgroundDirected strain evolution restructures metabolism for 1-butanol production in minimal media
Pontrelli, S., Fricke, R., Sakurai, S. S. M., Putri, S. P., Fitz‐Gibbon, S. T., Chung, M., Wu, H., Chen, Y., Pellegrini, M. A., Fukusaki, E., et al. (2018) · Metabolic Engineering · doi:10.1016/j.ymben.2018.08.004 · Cited by 27
Harper, M., Chen, Z., Toy, T. L., Machado, I. M. P., Nelson, S. F., Liao, J. C., & Lee, C. J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016517 · Cited by 26
“From this point of view, the easiest cases appear to be strains evolved without artificial mutagenesis, which typically contain only 10 - 20 mutations per bacterial genome [17] [30] [28] [19] [22] [7] , with in some cases as few as 3 mutations per strain [15] [10] or more than 40 [29] .”
Backgroundde Kok, S., Nijkamp, J. F., Oud, B., Roque, F. C., de Ridder, D., Daran, J.-M. G., Pronk, J. T., & van Maris, A. J. A. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2012.00787.x · Cited by 25
Improving Influenza HA-Vlps Production in Insect High Five Cells via Adaptive Laboratory Evolution
Correia, R., Fernandes, B., Alves, P. M., Carrondo, M. J. T., & Roldão, A. (2020) · Vaccines · doi:10.3390/vaccines8040589 · Cited by 24
“Besides improving cell growth [15] by enabling beneficial mutations to arise [16], this process also leads to more efficient energy utilization, the use of non-conventional substrates [17], tolerance to byproducts of interest [18,19], or even the development of thermo-resistant strains [20].”
BackgroundGenetic Diversity for Accelerating Microbial Adaptive Laboratory Evolution
Zheng, Y., Hong, K., Wang, B., Liu, D., Chen, T., & Wang, Z. (2021) · ACS Synthetic Biology · doi:10.1021/acssynbio.0c00589 · Cited by 24
Luo, J., McIntyre, E. A., Bedore, S. R., Santala, V. P., Neidle, E. L., & Santala, S. (2021) · Applied and Environmental Microbiology · doi:10.1128/aem.01780-21 · Cited by 22
Liu, Y., Wang, H., Li, S., Zhang, Y., Cheng, X., Xiang, W., & Wang, X. (2021) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-021-11164-7 · Cited by 23
Balola, A., Ferreira, S., & Rocha, I. (2024) · Metabolic Engineering Communications · doi:10.1016/j.mec.2024.e00254 · Cited by 22
Furusawa, C., Horinouchi, T., Hirasawa, T., & Shimizu, H. (2012) · Advances in biochemical engineering, biotechnology · doi:10.1007/10_2012_137 · Cited by 21
“coli cells [58].”
Yen, H., Li, F.-T., & Chang, J. (2013) · Bioresource Technology · doi:10.1016/j.biortech.2013.12.005 · Cited by 22
Phaneuf, P. V., Zielinski, D. C., Yurkovich, J. T., Johnsen, J., Szubin, R., Yang, L., Kim, S. H., Schulz, S., Wu, M., Dalldorf, C., et al. (2021) · ACS Synthetic Biology · doi:10.1021/acssynbio.1c00337 · Cited by 20
Self-citationNahku, R., Peebo, K., Valgepea, K., Barrick, J. E., Adamberg, K., & Vilu, R. (2011) · Microbiology · doi:10.1099/mic.0.050658-0 · Cited by 20
Adaptive Evolution of Thermotoga maritima Reveals Plasticity of the ABC Transporter Network
Latif, H., Şahin, M., Tarasova, J., Tarasova, Y., Portnoy, V. A., Nogales, J., & Zengler, K. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.01365-15 · Cited by 18
“Prolonged exposure to a perturbed environment such as elevated growth temperatures (14, 15) or exposure to a nonnative carbon source (16) may result in adapted regulation and/or genetic changes that result in improved phenotypic properties.”
BackgroundROS mediated selection for increased NADPH availability in Escherichia coli
Reynolds, T. S., Courtney, C. M., Erickson, K. E., Wolfe, L. M., Chatterjee, A., Nagpal, P., & Gill, R. T. (2017) · Biotechnology and Bioengineering · doi:10.1002/bit.26385 · Cited by 18
“(Glebes et al. 2017; Lee and Palsson 2010; Tenaillon et al. 2012) Finding mutations related to the phenotype of interest in adaptive evolution is entirely dependent on the selection used.”
Mahan, K. M., Penrod, J. T., Ju, K., Kass, N. A., Tan, W. A., Truong, R., Parales, J. V., & Parales, R. E. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.02772-14 · Cited by 18
“Bacteria are known for the ability to adapt to the presence of non-native carbon 539 and energy sources (54, 55).”
BackgroundEvolutionary design principles in metabolism
Sambamoorthy, G., Sinha, H., & Raman, K. (2019) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2019.0098 · Cited by 20
Improving glucose and xylose assimilation in Azotobacter vinelandii by adaptive laboratory evolution
Millán, C., Peña, C., Flores, C., Espı́n, G., Galindo, E., & Castillo, T. (2020) · World Journal of Microbiology and Biotechnology · doi:10.1007/s11274-020-02822-5 · Cited by 17
O’Boyle, N., Connolly, J. P. R., Tucker, N. P., & Roe, A. J. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2004977117 · Cited by 15
“coli adapts to stress (43–45) and can acquire the ability to derive nutrition from noncanonical carbon sources (46, 47).”
BackgroundConstructing and Analyzing Metabolic Flux Models of Microbial Communities
Faria, J. P., Khazaei, T., Edirisinghe, J., Weisenhorn, P., Seaver, S. M. D., Conrad, N., Harris, N., DeJongh, M., & Henry, C. (2016) · Springer protocols handbooks/Springer protocols · doi:10.1007/8623_2016_215 · Cited by 11
Yang, D., Rusch, L. M., Widney, K. A., Morgenthaler, A. B., & Copley, S. D. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2316834121 · Cited by 17
Recent Advances in Microbial Cell Growth Regulation Strategies for Metabolic Engineering
Noh, M. H., Cha, S., Kim, M., & Jung, G. Y. (2020) · Biotechnology and Bioprocess Engineering · doi:10.1007/s12257-019-0511-x · Cited by 16
Metadata
- Authors
- Lee, D.-H., & Palsson, B. Ø.
- Affiliations
- University of California San Diego (US)
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2010-07
- Volume
- 76
- Issue
- 13
- Pages
- 4158-4168
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- PMC
- PMC2897412
- OpenAlex
- W2135829725
- Cited by
- 160
- References
- 59
- Citations by year
- 2026: 6 · 2025: 7 · 2024: 6 · 2023: 4 · 2022: 8 · 2021: 15 · 2020: 13 · 2019: 7 · 2018: 8 · 2017: 7 · 2016: 9 · 2015: 16 · 2014: 9 · 2013: 13 · 2012: 14
- FWCI
- 8.10
- Type
- journal article
- Language
- en
- Update notices
- correction (2010-09-15)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Energy (FC02-02ER63446)
- National Institutes of Health
- Office of Science
- University of California, San Diego
- National Institute of General Medical Sciences (R01GM062791, GM 062791)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- Escherichia coli MG1655, adaptive evolution, whole-genome resequencing, growth rate, microbial evolution
- MeSH terms
- Adaptation, Physiological, Culture Media, DNA, Bacterial, Mutation, Polymerase Chain Reaction, Genome, Bacterial, Sequence Analysis, DNA, Directed Molecular Evolution, Propylene Glycol, Escherichia coli K12
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