The DOI matches its Crossref record; 59 of the 59 references it cites were found in a registry or an index.
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
Citations
Cites
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.
Datsenko, K., & Wanner, B. (2000) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.120163297 · Cited by 15,902
Escherichia coli and Salmonella :cellular and molecular biology
Neidhardt, F. C. (1996) · ASM Press eBooks · Cited by 8,197
The Neutral Theory of Molecular Evolution
Kimura, M. (1979) · Scientific American · doi:10.1038/scientificamerican1179-98 · Cited by 7,687
A constant rate of spontaneous mutation in DNA-based microbes.
Drake, J. W. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.16.7160 · Cited by 1,199
Genome evolution and adaptation in a long-term experiment with Escherichia coli
Barrick, J. E., Yu, D. S., Yoon, S. H., Jeong, H., Oh, T. K., Schneider, D., Lenski, R. E., & Kim, J. F. (2009) · Nature · doi:10.1038/nature08480 · Cited by 1,184
Characterization of the 1918 influenza virus polymerase genes
Taubenberger, J. K., Reid, A. H., Lourens, R. M., Wang, R., Jin, G., & Fanning, T. G. (2005) · Nature · doi:10.1038/nature04230 · Cited by 1,054
Integrating high-throughput and computational data elucidates bacterial networks
Covert, M. W., Knight, E. M., Reed, J. L., Herrgard, M. J., & Palsson, B. O. (2004) · Nature · doi:10.1038/nature02456 · Cited by 792
Self-citationThe mechanisms of carbon catabolite repression in bacteria
Deutscher, J. (2008) · Current Opinion in Microbiology · doi:10.1016/j.mib.2008.02.007 · Cited by 676
The origin of the naked grains of maize
Wang, H., Wagler, T. N., Li, B., Zhao, Q., Vigouroux, Y., Faller, M., Bomblies, K., LUKENS, L. N., & Doebley, J. (2005) · Nature · doi:10.1038/nature03863 · Cited by 603
Systematic changes in gene expression patterns following adaptive evolution in yeast
Ferea, T., Botstein, D., Brown, P. O., & Rosenzweig, R. F. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.17.9721 · Cited by 479
Calibrating bacterial evolution.
Ochman, H., Elwyn, S., & Moran, N. (1999) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.96.22.12638 · Cited by 457
Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli
Cooper, T. F., Rozen, D. E., & Lenski, R. E. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0334340100 · Cited by 440
Brückner, R., & Titgemeyer, F. (2002) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2002.tb11123.x · Cited by 413
Herring, C. D., Raghunathan, A., Honisch, C., Patel, T., Applebee, M. K., Joyce, A. R., Albert, T. J., Blattner, F. R., van den Boom, D., Cantor, C. R., et al. (2006) · Nature Genetics · doi:10.1038/ng1906 · Cited by 381
Self-citationThe Neutral Theory of Molecular Evolution
Ninio, J. (1984) · FEBS Letters · doi:10.1016/0014-5793(84)81411-8 · Cited by 313
Fong, S. S., Joyce, A. R., & Palsson, B. Ø. (2005) · Genome Research · doi:10.1101/gr.3832305 · Cited by 265 · cited 4×
“Compared to experimental evolution with native carbon sources, microorganisms might be more capable of adapting to various nonnative carbon compounds because microorganisms are able to adapt to environmental changes by using a number of strategies to meet their growth requirements and to achieve optimal overall perfor…”
BackgroundResultInfluentialSelf-citationInsertion of DNA activates the cryptic bgl operon in E. coli K12
Reynolds, A. E., Felton, J., & Wright, A. (1981) · Nature · doi:10.1038/293625a0 · Cited by 255
Hogema, B. M., Arents, J. C., Bader, R., Eijkemans, K., Yoshida, H., Takahashi, H., Aiba, H., & Postma, P. W. (1998) · Molecular Microbiology · doi:10.1046/j.1365-2958.1998.01053.x · Cited by 219
New Genes Implicated in the Protection of Anaerobically Grown Escherichia coli against Nitric Oxide
Justino, M. C., Vicente, J. B., Teixeira, M. S., & Saraiva, L. M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m411070200 · Cited by 210
Evolution of Drug Resistance in Experimental Populations of Candida albicans
Cowen, L. E., Sanglard, D., Calabrese, D., Sirjusingh, C., Anderson, J. B., & Kohn, L. M. (2000) · Journal of Bacteriology · doi:10.1128/jb.182.6.1515-1522.2000 · Cited by 207
Fong, S. S., Nanchen, A., Palsson, B. Ø., & Sauer, U. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m510016200 · Cited by 189
Self-citationComprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor
Velicer, G. J., Raddatz, G., Keller, H., Deiss, S., Lanz, C., Dinkelacker, I., & Schuster, S. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510740103 · Cited by 178
Gene replacement without selection: regulated suppression of amber mutations in Escherichia coli
Herring, C. D., Glasner, J. D., & Blattner, F. R. (2003) · Gene · doi:10.1016/s0378-1119(03)00585-7 · Cited by 177
Molecular basis of valine resistance in Escherichia coli K-12.
Lawther, R. P., Calhoun, D. H., Adams, C. W., Hauser, C. A., Gray, J. E., & Hatfield, G. W. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.2.922 · Cited by 175
Dynamics of insertion sequence elements during experimental evolution of bacteria
Schneider, D., & Lenski, R. E. (2004) · Research in Microbiology · doi:10.1016/j.resmic.2003.12.008 · Cited by 165
Biosynthesis of the Branched-Chain Amino Acids
Fink, P. S. (2014) · ASM Press eBooks · doi:10.1128/9781555818388.ch22 · Cited by 159
Fitness Evolution and the Rise of Mutator Alleles in Experimental Escherichia coli Populations
Shaver, A. C., Dombrowski, P. G., Sweeney, J. Y., Treis, T., Zappala, R. M., & Sniegowski, P. (2002) · Genetics · doi:10.1093/genetics/162.2.557 · Cited by 139
Directed Evolution of Ionizing Radiation Resistance in Escherichia coli
Harris, D. R., Pollock, S. V., Wood, E. A., Goiffon, R., Klingele, A. J., Cabot, E. L., Schackwitz, W., Martin, J., Eggington, J. M., Durfee, T. J., et al. (2009) · Journal of Bacteriology · doi:10.1128/jb.00502-09 · Cited by 136
Adaptation Limits Diversification of Experimental Bacterial Populations
Buckling, A. G. J., Wills, M. A., & Colegrave, N. (2003) · Science · doi:10.1126/science.1088848 · Cited by 134
Cocks, G. T., Aguilar, J., & Lin, E. C. C. (1974) · Journal of Bacteriology · doi:10.1128/jb.118.1.83-88.1974 · Cited by 117
Riehle, M. M., Bennett, A. F., Lenski, R. E., & Long, A. D. (2003) · Physiological Genomics · doi:10.1152/physiolgenomics.00034.2002 · Cited by 103
Sridhara, S., Wu, T. T., Chused, T. M., & Lin, E. C. C. (1969) · Journal of Bacteriology · doi:10.1128/jb.98.1.87-95.1969 · Cited by 97
Catabolite repression by glucose 6‐phosphate, gluconate and lactose in Escherichia coli
Hogema, B. M., Arents, J. C., Inada, T., Aiba, H., DAM, K. V., & Postma, P. W. (1997) · Molecular Microbiology · doi:10.1046/j.1365-2958.1997.3991761.x · Cited by 77
Wick, L. M., Weilenmann, H.-U., & Egli, T. W. (2002) · Microbiology · doi:10.1099/00221287-148-9-2889 · Cited by 69
Metabolic Characterization of Escherichia coli Strains Adapted to Growth on Lactate
Hua, Q., Joyce, A. R., Palsson, B. Ø., & Fong, S. S. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00527-07 · Cited by 67
Self-citationChen, Y. M., Lü, Z., & Lin, E. C. C. (1989) · Journal of Bacteriology · doi:10.1128/jb.171.11.6097-6105.1989 · Cited by 62
Hacking, A. J., & Lin, E. C. C. (1976) · Journal of Bacteriology · doi:10.1128/jb.126.3.1166-1172.1976 · Cited by 59
Cabiscol, E., Aguilar, J., & Ros, J. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)37413-6 · Cited by 55
Caballero, E., Baldomà, L., Ros, J., Boronat, A., & Aguilar, J. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)32248-8 · Cited by 52
Hall, B. G. (1976) · Journal of Molecular Biology · doi:10.1016/s0022-2836(76)80018-6 · Cited by 50
Transposable elements as activators of cryptic genes in E. coli
Hall, B. G. (1999) · Genetica · doi:10.1023/a:1003936706129 · Cited by 49
Protein Folding by Domain V of Escherichia coli 23S rRNA: Specificity of RNA-Protein Interactions
Samanta, D., Mukhopadhyay, D., Chowdhury, S., Ghosh, J., Pal, S. K., Basu, A., Bhattacharya, A., Das, A., Das, D., & DasGupta, C. K. (2008) · Journal of Bacteriology · doi:10.1128/jb.01800-07 · Cited by 48
Lewis, N. E., Cho, B., Knight, E. M., & Palsson, B. Ø. (2009) · Journal of Bacteriology · doi:10.1128/jb.00034-09 · Cited by 48
Self-citationEppler, T., & Boos, W. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01570.x · Cited by 45
Zeyl, C. (2005) · Genetics · doi:10.1534/genetics.104.027102 · Cited by 44
High-throughput mutation detection underlying adaptive evolution of Escherichia coli-K12Preprint
Honisch, C., Raghunathan, A., Cantor, C. R., Palsson, B. Ø., & van den Boom, D. (2004) · Genome Research · doi:10.1101/gr.2977704 · Cited by 40
Self-citationSecond naturally occurring β-galactosidase in E. coli
Hartl, D. L., & Hall, B. G. (1974) · Nature · doi:10.1038/248152a0 · Cited by 36
Hacking, A. J., & Lin, E. C. C. (1977) · Journal of Bacteriology · doi:10.1128/jb.130.2.832-838.1977 · Cited by 35
Rho-dependent transcriptional polarity in the ilvGMEDA operon of wild-type Escherichia coli K12.
Wek, R. C., Sameshima, J. H., & Hatfield, G. W. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)48168-9 · Cited by 33
Isolation of a mutation resulting in constitutive synthesis of L-fucose catabolic enzymes
Bartkus, J. M., & Mortlock, R. P. (1986) · Journal of Bacteriology · doi:10.1128/jb.165.3.710-714.1986 · Cited by 33
Evolution of an Escherichia coli Protein with Increased Resistance to Oxidative Stress
Lü, Z., Cabiscol, E., Obradors, N., Tamarit, J., Ros, J., Aguilar, J., & Lin, E. C. C. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.14.8308 · Cited by 33
Aronson, B., Levinthal, M., & Somerville, R. L. (1989) · Journal of Bacteriology · doi:10.1128/jb.171.10.5503-5511.1989 · Cited by 30
Catabolite repression: a story without end
Ullmann, A. (1996) · Research in Microbiology · doi:10.1016/0923-2508(96)83999-4 · Cited by 29
Gray, J. E., Patin, D. W., & Calhoun, D. H. (1981) · Molecular and General Genetics MGG · doi:10.1007/bf00268761 · Cited by 29
L-1,2-propanediol exits more rapidly than L-lactaldehyde from Escherichia coli
Zhu, Y., & Lin, E. C. C. (1989) · Journal of Bacteriology · doi:10.1128/jb.171.2.862-867.1989 · Cited by 23
An experiment in enzyme evolution studies with Pseudomonas aeruginosa amidase
Clarke, P. H., & Drew, R. E. (1988) · Bioscience Reports · doi:10.1007/bf01116455 · Cited by 23
Sanyal, S. C. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.11.2390 · Cited by 19
Podolny, V., Lin, E. C. C., & Hochschild, A. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.24.7457-7463.1999 · Cited by 12
Inactivation of propanediol oxidoreductase of Escherichia coli by metal-catalyzed oxidation
Cabiscol, E., Badı́a, J., Baldomà, L., Hidalgo, E., Aguilar, J., & Ros, J. (1992) · Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology · doi:10.1016/0167-4838(92)90144-3 · Cited by 10
Cited by
Sorted by citations
Adaptive laboratory evolution—Principles and applications for biotechnology
Dragosits, M., & Mattanovich, D. (2013) · Microbial Cell Factories · doi:10.1186/1475-2859-12-64 · Cited by 827
“coli culture could evolve the ability to aerobically utilize citrate [37], or the ability to use the non-natural carbon source 1,2-propanediol [71]; also, a strain deficient in glutathione biosynthesis was able to develop compensatory mutations to restore this function [147].”
BackgroundKawecki, T. J., Lenski, R. E., Ebert, D., Hollis, B., Olivieri, I., & Whitlock, M. C. (2012) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2012.06.001 · Cited by 807
Sandberg, T. E., Salazar, M. J., Weng, L. L., Palsson, B. Ø., & Feist, A. M. (2019) · Metabolic Engineering · doi:10.1016/j.ymben.2019.08.004 · Cited by 585
Self-citationBasic and applied uses of genome‐scale metabolic network reconstructions of Escherichia coli
McCloskey, D., Palsson, B. Ø., & Feist, A. M. (2013) · Molecular Systems Biology · doi:10.1038/msb.2013.18 · Cited by 327
“These changes can then be reintroduced and their effect on the organism’s fitness studied (Herring et al , 2006; Conrad et al , 2009; Lee and Palsson, 2010; Applebee et al , 2011).”
BackgroundSelf-citationAdaptive laboratory evolution — harnessing the power of biology for metabolic engineering
Portnoy, V. A., Bezdan, D., & Zengler, K. (2011) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2011.03.007 · Cited by 309
“(d) and (e) Activation of ‘latent’ pathways by forcing the microorganism to utilize or produce nonnative substrates leads to valuable biological discoveries [3,32].”
BackgroundMethod
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review