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.
Integrity signals
Registry
Cites
Statistics
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?
Certain environments can lead to fast selection of improved phenotypes, whereas others, including long-term adaptation to environmental pH, represent complex environments where microbial cells show low adaptive potential in terms of absolute fitness gain.
“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]
Gene amplifications were identified to contribute to increased gene dosage and subsequently increased fitness.
“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]
Frequent rpoB mutations were found during batch evolution on glucose in E. coli.
“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]
Increased growth during osmotic stress in E. coli was linked to mutations that led to increased expression of enterobactin biosynthesis genes, including fepA and entD.
“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]
The rpoS mutation alone did not positively influence the growth rate in the ancestral ∆pgi E. coli strain; rpoS mutations were epistatically linked to additional mutations.
“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]
Mutations in acrAB and marC were found independently in studies of iso- and n-butanol stress in E. coli; further changes were linked to carbon and nitrogen metabolism via gatY and tnaA, enterobactin synthesis, or attenuated rpoS activity via hfq mutations.
“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]
n-butanol tolerance in E. coli is weakly compatible with oxidative stress and leads to trade-offs in hexane and chloramphenicol resistance.
“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]
n-butanol tolerance was reported to be highly compatible with osmotic stress.
“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]
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).
“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]
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 · see citing works
Escherichia coli and Salmonella :cellular and molecular biology
Neidhardt, F. C. (1996) · ASM Press eBooks · Cited by 8,197 · see citing works
The Neutral Theory of Molecular Evolution
Kimura, M. (1979) · Scientific American · doi:10.1038/scientificamerican1179-98 · Cited by 7,698 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Brückner, R., & Titgemeyer, F. (2002) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2002.tb11123.x · Cited by 413 · see citing works
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 · see citing works
Self-citationThe Neutral Theory of Molecular Evolution
Ninio, J. (1984) · FEBS Letters · doi:10.1016/0014-5793(84)81411-8 · Cited by 313 · see citing works
Fong, S. S., Joyce, A. R., & Palsson, B. Ø. (2005) · Genome Research · doi:10.1101/gr.3832305 · Cited by 265 · cited 4× · see citing works
“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 · see citing works
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 · see citing works
Evolution of Drug Resistance in Experimental Populations of <i>Candida albicans</i>
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 · see citing works
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 205 · see citing works
Fong, S. S., Nanchen, A., Palsson, B. Ø., & Sauer, U. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m510016200 · Cited by 189 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Biosynthesis of the Branched-Chain Amino Acids
Fink, P. S. (2014) · ASM Press eBooks · doi:10.1128/9781555818388.ch22 · Cited by 157 · see citing works
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 138 · see citing works
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 · see citing works
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 132 · see citing works
Cocks, G. T., Aguilar, J., & Lin, E. C. C. (1974) · Journal of Bacteriology · doi:10.1128/jb.118.1.83-88.1974 · Cited by 121 · see citing works
Riehle, M. M., Bennett, A. F., Lenski, R. E., & Long, A. D. (2003) · Physiological Genomics · doi:10.1152/physiolgenomics.00034.2002 · Cited by 103 · see citing works
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 · see citing works
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 · see citing works
Wick, L. M., Weilenmann, H.-U., & Egli, T. W. (2002) · Microbiology · doi:10.1099/00221287-148-9-2889 · Cited by 69 · see citing works
Metabolic Characterization of <i>Escherichia coli</i> 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 · see citing works
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 · see citing works
Hacking, A. J., & Lin, E. C. C. (1976) · Journal of Bacteriology · doi:10.1128/jb.126.3.1166-1172.1976 · Cited by 59 · see citing works
Cabiscol, E., Aguilar, J., & Ros, J. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)37413-6 · Cited by 54 · see citing works
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 · see citing works
Hall, B. G. (1976) · Journal of Molecular Biology · doi:10.1016/s0022-2836(76)80018-6 · Cited by 50 · see citing works
Transposable elements as activators of cryptic genes in E. coli
Hall, B. G. (1999) · Genetica · doi:10.1023/a:1003936706129 · Cited by 49 · see citing works
Lewis, N. E., Cho, B., Knight, E. M., & Palsson, B. Ø. (2009) · Journal of Bacteriology · doi:10.1128/jb.00034-09 · Cited by 49 · see citing works
Self-citationProtein 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 46 · see citing works
Eppler, T., & Boos, W. (1999) · Molecular Microbiology · doi:10.1046/j.1365-2958.1999.01570.x · Cited by 45 · see citing works
Zeyl, C. (2005) · Genetics · doi:10.1534/genetics.104.027102 · Cited by 44 · see citing works
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 · see citing works
Self-citationSecond naturally occurring β-galactosidase in E. coli
Hartl, D. L., & Hall, B. G. (1974) · Nature · doi:10.1038/248152a0 · Cited by 36 · see citing works
Hacking, A. J., & Lin, E. C. C. (1977) · Journal of Bacteriology · doi:10.1128/jb.130.2.832-838.1977 · Cited by 35 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Aronson, B., Levinthal, M., & Somerville, R. L. (1989) · Journal of Bacteriology · doi:10.1128/jb.171.10.5503-5511.1989 · Cited by 30 · see citing works
Catabolite repression: a story without end
Ullmann, A. (1996) · Research in Microbiology · doi:10.1016/0923-2508(96)83999-4 · Cited by 29 · see citing works
Gray, J. E., Patin, D. W., & Calhoun, D. H. (1981) · Molecular and General Genetics MGG · doi:10.1007/bf00268761 · Cited by 29 · see citing works
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 · see citing works
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 · see citing works
Sanyal, S. C. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.11.2390 · Cited by 19 · see citing works
Podolny, V., Lin, E. C. C., & Hochschild, A. (1999) · Journal of Bacteriology · doi:10.1128/jb.181.24.7457-7463.1999 · Cited by 12 · see citing works
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 · see citing works
Flagged first, then by citations
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 · see citing works
“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 · see citing works
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 558 · see citing works
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 317 · see citing works
“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 · see citing works
“(d) and (e) Activation of ‘latent’ pathways by forcing the microorganism to utilize or produce nonnative substrates leads to valuable biological discoveries [3,32].”
BackgroundMethodNetwork Context and Selection in the Evolution to Enzyme Specificity
Nam, H., Lewis, N. E., Lerman, J. A., Lee, D.-H., Chang, R. L., Kim, D., & Palsson, B. O. (2012) · Science · doi:10.1126/science.1216861 · Cited by 277 · see citing works
Self-citationMonk, J. M., Charusanti, P., Aziz, R. K., Lerman, J. A., Premyodhin, N., Orth, J. D., Feist, A. M., & Palsson, B. Ø. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1307797110 · Cited by 286 · see citing works
“Adaptive laboratory evolution of these two strains on D-malate may relieve the transcriptional repression of yeaU and lead to identification of novel regulators involved in controlling the catabolism of this compound (36).”
BackgroundSelf-citationMicrobial laboratory evolution in the era of genome‐scale science
Conrad, T. M., Lewis, N. E., & Palsson, B. Ø. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.42 · Cited by 279 · see citing works
“In the studies summarized in Figure 1 (Herring et al, 2006; Barrick et al, 2009; Conrad et al, 2009; Charusanti et al, 2010; Kishimoto et al, 2010; Lee and Palsson, 2010), single-nucleotide mutations were the most common type of mutation observed (61% of observed mutations) and c4t/g4a mutations…”
BackgroundInfluentialSelf-citationLaCroix, R. A., Sandberg, T. E., O'Brien, E. J., Utrilla, J., Ebrahim, A., Guzmán, G. I., Szubin, R., Palsson, B. Ø., & Feist, A. M. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.02246-14 · Cited by 254 · see citing works
“Similar continuous exponential-growth-phase ALE experiments run for 10(11) CCDs (more than an order of magnitude fewer than in the present study) on glycerol, lactic acid, and L-1,2-propanediol minimal media yielded 2 to 5, 1 to 8, and 5 to 6 mutations per independent experiment, respectively (23, 24, 45).”
BackgroundSelf-citationJensen, P. A., & Papin, J. A. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq702 · Cited by 226 · see citing works
Zymomonas mobilis: a novel platform for future biorefineries
He, M., Wu, B., Qin, H., Ruan, Z., Tan, F., Wang, J., Shui, Z., Dai, L., Zhu, Q., Pan, K., et al. (2014) · Biotechnology for Biofuels · doi:10.1186/1754-6834-7-101 · Cited by 203 · see citing works
Engineering Escherichia coli for methanol conversion
Müller, J. E. N., Meyer, F., Litsanov, B., Kiefer, P., Potthoff, E., Heux, S., Quax, W. J., Wendisch, V. F., Brautaset, T., Portais, J., et al. (2015) · Metabolic Engineering · doi:10.1016/j.ymben.2014.12.008 · Cited by 203 · see citing works
“Such approaches have been applied successfully if basal activity of the enzymes or pathways could be established (Lee and Palsson, 2010).”
Li, D., Zeng, S., He, M., & Gu, A. Z. (2016) · Environmental Science & Technology · doi:10.1021/acs.est.5b05113 · Cited by 193 · see citing works
New insights into bacterial adaptation through in vivo and in silico experimental evolution
Hindré, T., Knibbe, C., Beslon, G., & Schneider, D. (2012) · Nature Reviews Microbiology · doi:10.1038/nrmicro2750 · Cited by 184 · see citing works
“First, major phenotypic inno vations can emerge, including the ability to colonize eco logical niches that are not used by the ancestor 23,55 ; new growth, metabolic and resistance abilities 39,41,49,50,52,53,56–58 ; and the mobilization of new or unused cellular path ways 22,24,31–34 .”
BackgroundMinty, 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., et al. (2011) · Microbial Cell Factories · doi:10.1186/1475-2859-10-18 · Cited by 185 · see citing works
“coli in several experimental evolutions studies, including short-term evolution on glycerol, lactate, and L-1,2-propanediol carbon sources, adaptation to high radiation levels, and long-term genome evolution over 40,000 generations [16-20].”
BackgroundRandom sequences rapidly evolve into de novo promoters
Yona, A. H., Alm, E. J., & Gore, J. (2018) · Nature Communications · doi:10.1038/s41467-018-04026-w · Cited by 182 · see citing works
Wielgoss, S., Barrick, J. E., Tenaillon, O., Cruveiller, S., Chane-Woon-Ming, B., Médigue, C., Lenski, R. E., & Schneider, D. (2011) · G3 Genes Genomes Genetics · doi:10.1534/g3.111.000406 · Cited by 177 · see citing works
Adaptive laboratory evolution of a genome-reduced Escherichia coli
Choe, D., Lee, J. H., Yoo, M., Hwang, S., Sung, B. H., Cho, S., Palsson, B. Ø., Kim, S. C., & Cho, B. (2019) · Nature Communications · doi:10.1038/s41467-019-08888-6 · Cited by 162 · see citing works
Self-citationEvolutionary insight from whole‐genome sequencing of experimentally evolved microbes
DETTMAN, J. R., RODRIGUE, N., MELNYK, A. H., WONG, A., BAILEY, S. F., & KASSEN, R. (2012) · Molecular Ecology · doi:10.1111/j.1365-294x.2012.05484.x · Cited by 160 · see citing works
“…of synergistic (positive) epistasis, where the fitness effect of mutations in combination is greater than would be expected from the sum of their independent effects (Herring et al. 2006; Applebee et al. 2008; Conrad et al. 2009; Anderson et al. 2010; Lee & Palsson 2010; Minty et al. 2011).”
BackgroundInfluentialEngineering Corynebacterium glutamicum for methanol-dependent growth and glutamate production
Tuyishime, P., Wang, Y., Fan, L., Zhang, Q., Li, Q., Zheng, P., Sun, J., & Ma, Y. (2018) · Metabolic Engineering · doi:10.1016/j.ymben.2018.07.011 · Cited by 151 · see citing works
Kim, Y.-H., Lama, S., Agrawal, D., Kumar, V., & Park, S. (2021) · Biotechnology Advances · doi:10.1016/j.biotechadv.2021.107736 · Cited by 142 · see citing works
Genetic Basis of Growth Adaptation of Escherichia coli after Deletion of pgi, a Major Metabolic Gene
Charusanti, P., Conrad, T. M., Knight, E. M., Venkataraman, K., Fong, N. L., Xie, B., Gao, Y., & Palsson, B. Ø. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001186 · Cited by 135 · see citing works
Self-citationBiosensor‐Enabled Directed Evolution to Improve Muconic Acid Production in Saccharomyces cerevisiae
Leavitt, J. M., Wagner, J. M., Tu, C. C., Tong, A., Liu, Y., & Alper, H. S. (2017) · Biotechnology Journal · doi:10.1002/biot.201600687 · Cited by 132 · see citing works
Current Status and Applications of Adaptive Laboratory Evolution in Industrial Microorganisms
Lee, S., & Kim, P. (2020) · Journal of Microbiology and Biotechnology · doi:10.4014/jmb.2003.03072 · Cited by 127 · see citing works
Biological production of adipic acid from renewable substrates: Current and future methods
Deng, Y., Ma, L., & Mao, Y. (2015) · Biochemical Engineering Journal · doi:10.1016/j.bej.2015.08.015 · Cited by 127 · see citing works
White biotechnology: State of the art strategies for the development of biocatalysts for biorefining
Heux, S., Meynial‐Salles, I., O’Donohue, M. J., & Dumon, C. (2015) · Biotechnology Advances · doi:10.1016/j.biotechadv.2015.08.004 · Cited by 120 · see citing works
“…(Zhang et al. , 2009), (ii) adapt microorganisms to growth on alternative carbon sources (Balderas-Hernandez et al. , 2011, Conrad et al. , 2009, Lee and Palsson, 2010), (iii) evolve E. coli MG1655 in mineral medium containing excess glucose (LaCroix et al. , 2015) and (iv) improve lipogenesis…”
BackgroundReyes, L. H., Almario, M. P., Winkler, J. D., Orozco, M. M., & Kao, K. C. (2012) · Metabolic Engineering · doi:10.1016/j.ymben.2012.05.002 · Cited by 112 · see citing works
A Model for Designing Adaptive Laboratory Evolution Experiments
LaCroix, R. A., Palsson, B. Ø., & Feist, A. M. (2017) · Applied and Environmental Microbiology · doi:10.1128/aem.03115-16 · Cited by 103 · see citing works
“A more in-depth retrospective analysis revealed 93 similar trends where passage amounts were significantly decreased (14-18).”
BackgroundSelf-citationBacterial growth rate reflects a bottleneck in resource allocation
Goelzer, A., & Fromion, V. (2011) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2011.05.014 · Cited by 102 · see citing works
Jahn, L. J., Munck, C., Ellabaan, M. M. H., & Sommer, M. O. A. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00816 · Cited by 102 · see citing works
“ALE can be utilized to improve production strains by increasing their tolerance to the metabolic product (Hu et al., 2016; Lennen, 2016), by activating latent pathways (Wang et al., 2016) or by enabling the utilization of non-native substrates (Lee and Palsson, 2010).”
BackgroundMethodModel-driven discovery of underground metabolic functions in Escherichia coli
Guzmán, G. I., Utrilla, J., Nurk, S., Brunk, E., Monk, J. M., Ebrahim, A., Palsson, B. Ø., & Feist, A. M. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1414218112 · Cited by 92 · see citing works
“To promote growth, a “weaning” ALE was performed (36).”
MethodSelf-citationCurrent status and future prospective of bio-ethanol industry in China
Wu, B., Wang, Y., Dai, Y., Song, C., Zhu, Q., Qin, H., Tan, F., Chen, C., Dai, L., Hu, G., et al. (2021) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2021.111079 · Cited by 96 · see citing works
Adaptive evolution of complex innovations through stepwise metabolic niche expansion
Szappanos, B., Fritzemeier, C. J., Csörgő, B., Lázár, V., Lu, X., Fekete, G., Bálint, B., Herczeg, R., Nagy, I., Notebaart, R. A., et al. (2016) · Nature Communications · doi:10.1038/ncomms11607 · Cited by 91 · see citing works
Singh, T. A., Devi, K. R., Ahmed, G., & Jeyaram, K. (2013) · Food Research International · doi:10.1016/j.foodres.2013.11.028 · Cited by 91 · see citing works
Long, C. P., Gonzalez, J. E., Feist, A. M., Palsson, B. Ø., & Antoniewicz, M. R. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1716056115 · Cited by 88 · see citing works
Self-citationExperimental Evolution of a Facultative Thermophile from a Mesophilic Ancestor
Blaby, I. K., Lyons, B. J., Wroclawska-Hughes, E., Phillips, G. C. F., Pyle, T. P., Chamberlin, S. G., Benner, S. A., Lyons, T. J., de Crécy‐Lagard, V., & de Crécy, E. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.05773-11 · Cited by 86 · see citing works
“However, the advent of new highthroughput sequencing methods has changed this dynamic (3, 5, 25), and experimental evolution is increasingly being recognized as a potent method for altering the phenotypes of industrially important microbes (11, 17).”
MethodAcid-Adapted Strains of Escherichia coli K-12 Obtained by Experimental Evolution
Harden, M. M., He, A., Creamer, K. E., Clark, M. W., Hamdallah, I., Martinez, K. A., Kresslein, R. L., Bush, S. P., & Slonczewski, J. L. (2015) · Applied and Environmental Microbiology · doi:10.1128/aem.03494-14 · Cited by 79 · see citing works
“the approach of experimental evolution (21, 22).”
Lescat, M., Launay, A., Ghalayini, M., Magnan, M., Glodt, J., Pintard, C., Dion, S., Denamur, É., & Tenaillon, O. (2016) · Molecular Ecology · doi:10.1111/mec.13851 · Cited by 81 · see citing works
Shui, Z.-X., Qin, H., Wu, B., Ruan, Z., Wang, L.-S., Tan, F., Wang, J., Tang, X., Dai, L., Hu, G., et al. (2015) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-015-6616-z · Cited by 80 · see citing works
Shi, A., Fan, F., & Broach, J. R. (2021) · Journal of Industrial Microbiology & Biotechnology · doi:10.1093/jimb/kuab076 · Cited by 77 · see citing works
Newly Identified Genetic Variations in Common Escherichia coli MG1655 Stock Cultures
Freddolino, L., Amini, S., & Tavazoie, S. (2011) · Journal of Bacteriology · doi:10.1128/jb.06087-11 · Cited by 76 · see citing works
“As seen in Table 1, the remaining three noted mutations (two point mutations in the ylbE pseudogene and an insertion in the ppiC-yifO intergenic region) were also present in the ancestral MG1655 strain (ATCC 47076/CGSC6300); all three were also recently noted to be present in MG1655 by Skovgaard et al. (22), and those…”
BackgroundTransfer of noncoding DNA drives regulatory rewiring in bacteria
Oren, Y., Smith, M. B., Johns, N. I., Zeevi, M. K., Biran, D., Ron, E. Z., Corander, J., Wang, H. H., Alm, E. J., & Pupko, T. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1413272111 · Cited by 75 · see citing works
Gerstein, A. C., Rosenberg, A., Hecht, I., & Berman, J. (2016) · Microbiology · doi:10.1099/mic.0.000295 · Cited by 63 · see citing works
Ma, K., Ruan, Z., Shui, Z.-X., Wang, Y., Hu, G., & He, M. (2015) · Bioresource Technology · doi:10.1016/j.biortech.2015.12.054 · Cited by 73 · see citing works
Lee, D., Feist, A. M., Barrett, C. L., & Palsson, B. Ø. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026172 · Cited by 71 · see citing works
Self-citationWang, G., Shi, T., Chen, T., Wang, X., Wang, Y., Liu, D., Guo, J., Fu, J., Feng, L., Wang, Z., et al. (2018) · Metabolic Engineering · doi:10.1016/j.ymben.2018.05.022 · Cited by 68 · see citing works
Kok, S., Nijkamp, J. F., Oud, B., Roque, F. C., Ridder, D., Daran, J.-M., Pronk, J. T., & Maris, A. J. A. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00787.x · Cited by 65 · see citing works
Long, C. P., Gonzalez, J. E., Feist, A. M., Palsson, B. Ø., & Antoniewicz, M. R. (2017) · Metabolic Engineering · doi:10.1016/j.ymben.2017.09.012 · Cited by 63 · see citing works
“…et al., 2010; Mundhada et al., 2017; Reyes et al., 2012), rates of growth on diverse substrates (Cordova et al., 2016; Herring et al., 2006; Lee and Palsson, 2010; Sandberg et al., 2017), and gaining general insight into microbial responses to environmental or genetic perturbations…”
BackgroundSelf-citationFunctional and Metabolic Effects of Adaptive Glycerol Kinase (GLPK) Mutants in Escherichia coli
Applebee, M. K., Joyce, A. R., Conrad, T. M., Pettigrew, D. W., & Palsson, B. Ø. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.195305 · Cited by 64 · see citing works
Self-citationUnderground metabolism: network-level perspective and biotechnological potential
Notebaart, R. A., Kintses, B., Feist, A. M., & Papp, B. (2017) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2017.07.015 · Cited by 62 · see citing works
Accelerating pathway evolution by increasing the gene dosage of chromosomal segments
Tumen-Velasquez, M. P., Johnson, C. W., Ahmed, A. R., Dominick, G., Fulk, E. M., Khanna, P., Lee, S. A., Schmidt, A. L., Linger, J. G., Eiteman, M. A., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1803745115 · Cited by 56 · see citing works
“Other effective methods (34, 35), which provide alternative carbon sources during adaptation to novel growth substrates, might have yielded Gua mutants.”
MethodEvolutionary Instability of Symbiotic Function in Bradyrhizobium japonicum
Sachs, J. L., Russell, J. E., & Hollowell, A. C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026370 · Cited by 56 · see citing works
Seong, W., Han, G. H., Lim, H. S., Baek, J. I., Kim, S.-J., Kim, D., Kim, S. K., Lee, H., Kim, H., Lee, S., et al. (2020) · Metabolic Engineering · doi:10.1016/j.ymben.2020.09.005 · Cited by 56 · see citing works
Self-citationEngineering Escherichia coli for the utilization of ethylene glycol
Pandit, A. V., Harrison, E., & Mahadevan, R. (2021) · Microbial Cell Factories · doi:10.1186/s12934-021-01509-2 · Cited by 55 · see citing works
Saez, J. M., Aparicio, J. D., Amoroso, M. J., & Benimeli, C. S. (2015) · Process Biochemistry · doi:10.1016/j.procbio.2015.08.014 · Cited by 52 · see citing works
Nguyen-Vo, T. P., Liang, Y., Sankaranarayanan, M., Seol, E., Chun, A. Y., Ashok, S., Chauhan, A. S., Kim, J. R., & Park, S. (2019) · Metabolic Engineering · doi:10.1016/j.ymben.2019.02.001 · Cited by 48 · see citing works
Phenotypic convergence in bacterial adaptive evolution to ethanol stress
Horinouchi, T., Suzuki, S., Hirasawa, T., Ono, N., Yomo, T., Shimizu, H., & Furusawa, C. (2015) · BMC Evolutionary Biology · doi:10.1186/s12862-015-0454-6 · Cited by 43 · see citing works
“…to adaptive phenotypic changes against various environments, including several carbon sources (Conrad, et al. 2009; Cooper and Lenski 2010; Lee and Palsson 2010), different temperatures (Kishimoto, et al. 2010; Tenaillon, et al. 2012), high ethanol (Goodarzi, et al. 2010) and isobutanol…”
BackgroundMichener, J. K., Neves, A. A. C., Vuilleumier, S., Bringel, F., & Marx, C. J. (2014) · eLife · doi:10.7554/elife.04279 · Cited by 43 · see citing works
“Meanwhile, metabolic engineers have used adaptive evolution as an engineering tool, including the evolution of highly modified strains, but under conditions that do not reproduce HGT ( Fong et al., 2005 ; Trinh and Srienc, 2009 ; Lee and Palsson, 2010 ; Lee et al., 2012 ).”
How adaptive evolution reshapes metabolism to improve fitness: recent advances and future outlook
Long, C. P., & Antoniewicz, M. R. (2018) · Current Opinion in Chemical Engineering · doi:10.1016/j.coche.2018.11.001 · Cited by 44 · see citing works
Underground isoleucine biosynthesis pathways in E. coli
Cotton, C. A. R., Bernhardsgrütter, I., He, H., Burgener, S., Schulz, L., Paczia, N., Dronsella, B. B., Erban, A., Toman, S., Dempfle, M., et al. (2020) · eLife · doi:10.7554/elife.54207 · Cited by 43 · see citing works
Experimental Evolution of Innovation and Novelty
Kassen, R. (2019) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2019.03.008 · Cited by 42 · see citing works
Anguluri, K., China, S. L., Brugnoli, M., Cassanelli, S., & Gullo, M. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.994097 · Cited by 40 · see citing works
“An alternative approach to genetic engineering strategy is the exploitation of adaptation mechanisms, developed by bacteria under predefined environmental conditions (Lee and Palsson, 2010; Barve and Wagner, 2013; Matsutani et al., 2013; Zorraquino et al., 2016).”
BackgroundSummers, Z. M., Ueki, T., Ismail, W., Haveman, S. A., & Lovley, D. R. (2012) · The ISME Journal · doi:10.1038/ismej.2011.166 · Cited by 39 · see citing works
Streamlining genomes: toward the generation of simplified and stabilized microbial systems
Leprince, A., van Passel, M. W. J., & dos Santos, V. A. P. M. (2012) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2012.05.001 · Cited by 37 · see citing works
“The optimization of genomes can also be performed by experimental evolution, selecting for favorable genotypes [49,50].”
BackgroundWytock, T. P., Fiebig, A., Willett, J. W., Herrou, J., Fergin, A., Motter, A. E., & Crosson, S. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007284 · Cited by 35 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
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 30 · see citing works
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 · see citing works
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 · see citing works
Kim, H. J., Turner, T. L., & Jin, Y. (2013) · Biotechnology Advances · doi:10.1016/j.biotechadv.2013.03.010 · Cited by 29 · see citing works
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 · see citing works
“…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 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
“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 · see citing works
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 · see citing works
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 · see citing works
Balola, A., Ferreira, S., & Rocha, I. (2024) · Metabolic Engineering Communications · doi:10.1016/j.mec.2024.e00254 · Cited by 22 · see citing works
Furusawa, C., Horinouchi, T., Hirasawa, T., & Shimizu, H. (2012) · Advances in biochemical engineering, biotechnology · doi:10.1007/10_2012_137 · Cited by 21 · see citing works
“coli cells [58].”
Yen, H., Li, F.-T., & Chang, J. (2013) · Bioresource Technology · doi:10.1016/j.biortech.2013.12.005 · Cited by 22 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
“(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 · see citing works
“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 18 · see citing works
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 · see citing works
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 18 · see citing works
“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 · see citing works
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 · see citing works
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 17 · see citing works
- 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
