Parallel Genetic and Phenotypic Evolution of DNA Superhelicity in Experimental Populations of Escherichia coli
Abstract
DNA supercoiling is the master function that interconnects chromosome structure and global gene transcription. This function has recently been shown to be under strong selection in Escherichia coli. During the evolution of 12 initially identical populations propagated in a defined environment for 20,000 generations, parallel increases in DNA supercoiling were observed in ten populations. The genetic changes associated with the increased supercoiling were examined in one population, and beneficial mutations in the genes topA (encoding topoisomerase I) and fis (encoding a histone-like protein) were identified. To elucidate the molecular basis and impact of these changes, we quantified the level of genetic, phenotypic, and molecular parallelism linked to DNA supercoiling in all 12 evolving populations. First, sequence determination of DNA topology-related loci revealed strong genetic parallelism, with mutations concentrated in three genes (topA, fis, and dusB), although the populations had different alleles at each locus. Statistical analyses of these polymorphisms implied the action of positive selection and, moreover, suggested that fis and dusB, which belong to the same operon, have related functions. Indeed, we demonstrated that DusB regulates the expression of fis by both experimental and phylogenetic analyses. Second, molecular analyses of five mutations in fis and dusB affecting the transcription, translation, and protein activity of Fis also revealed strong parallelism in the resulting phenotypic effects. Third, artificially increasing DNA supercoiling in one of the two populations that lacked DNA topology changes led to a significant fitness increase. The high levels of molecular and genetic parallelism, targeting a small subset of the many genes involved in DNA supercoiling, indicate that changes in DNA superhelicity have been important in the evolution of these populations. Surprisingly, however, most of the evolved alleles we tested had either no detectable or slightly deleterious effects on fitness, despite these signatures of positive selection.
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Gene duplications are a prerequisite for the development of novel molecular functions.
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The evolutionary mechanisms described in the preceding sections are crucial towards the development of species-specific specializations.
“The evolutionary mechanisms described in the preceding sections are crucial towards the development of such specializations [130,156,171].”
From Adaptive laboratory evolution—Principles and applications for biotechnology (2013) · cites this paper as [130]
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Feldman-Cohen, L. S., Shao, Y., Meinhold, D. W., Miller, C., Colón, W., & Osuna, R. (2006) · Journal of Bacteriology · doi:10.1128/jb.188.6.2081-2095.2006 · Cited by 23 · see citing works
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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
Genome dynamics during experimental evolution
Barrick, J. E., & Lenski, R. E. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3564 · Cited by 619 · see citing works
Self-citationSobetzko, P., TRAVERS, A. A., & Muskhelishvili, G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1108229109 · Cited by 203 · 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
Self-citationWong, A., Rodrigue, N., & Kassen, R. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002928 · Cited by 169 · see citing works
Maddamsetti, R., Lenski, R. E., & Barrick, J. E. (2015) · Genetics · doi:10.1534/genetics.115.176677 · Cited by 167 · 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
Deatherage, D. E., Kepner, J., Bennett, A. F., Lenski, R. E., & Barrick, J. E. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616132114 · Cited by 134 · see citing works
Self-citationLenski, R. E., Wiser, M. J., Ribeck, N., Blount, Z. D., Nahum, J., Morris, J., Zaman, L., Turner, C. B., Wade, B. D., Maddamsetti, R., et al. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.2292 · Cited by 127 · see citing works
Self-citationKinsler, G., Geiler‐Samerotte, K., & Petrov, D. A. (2020) · eLife · doi:10.7554/elife.61271 · Cited by 110 · see citing works
Consuegra, J., Gaffé, J., Lenski, R. E., Hindré, T., Barrick, J. E., Tenaillon, O., & Schneider, D. (2021) · Nature Communications · doi:10.1038/s41467-021-21210-7 · Cited by 116 · see citing works
Self-citationReplaying the Tape of Life: Quantification of the Predictability of Evolution
Lobkovsky, A. E., & Koonin, E. V. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00246 · Cited by 103 · see citing works
Rovinskiy, N., Agbleke, A. A., Chesnokova, O., Pang, Z., & Higgins, N. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002845 · Cited by 109 · see citing works
Cameron, A. D. S., Stoebel, D. M., & Dorman, C. J. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07560.x · Cited by 86 · see citing works
Pervasive regulation of nucleoid structure and function by nucleoid-associated proteins
Rimsky, S., & TRAVERS, A. A. (2011) · Current Opinion in Microbiology · doi:10.1016/j.mib.2011.01.003 · Cited by 82 · see citing works
Bullied no more: when and how DNA shoves proteins around
Fogg, J. M., Randall, G. L., Pettitt, B. M., Sumners, D. W., Harris, S. A., & Zechiedrich, L. (2012) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583512000054 · Cited by 76 · see citing works
Convergence and Divergence in a Long-Term Experiment with Bacteria
Lenski, R. E. (2017) · The American Naturalist · doi:10.1086/691209 · Cited by 72 · see citing works
Self-citationThe chromosomal accommodation and domestication of mobile genetic elements
Touchon, M., Bobay, L., & Rocha, E. P. C. (2014) · Current Opinion in Microbiology · doi:10.1016/j.mib.2014.09.010 · Cited by 70 · see citing works
Junier, I., & Rivoire, O. (2016) · PLoS ONE · doi:10.1371/journal.pone.0155740 · Cited by 66 · see citing works
Functional 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
Antibiotic-Independent Adaptive Effects of Antibiotic Resistance Mutations
Hershberg, R. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.05.003 · Cited by 53 · see citing works
Core Genes Evolve Rapidly in the Long-Term Evolution Experiment with Escherichia coli
Maddamsetti, R., Hatcher, P. J., Green, A. G., Williams, B. L., Marks, D. S., & Lenski, R. E. (2017) · Genome Biology and Evolution · doi:10.1093/gbe/evx064 · Cited by 53 · see citing works
Self-citationChromosomal position shift of a regulatory gene alters the bacterial phenotype
Gerganova, V., Berger, M., Zaldastanishvili, E., Sobetzko, P., Lafon, C., Mourez, M., TRAVERS, A. A., & Muskhelishvili, G. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv709 · Cited by 51 · see citing works
A case study in evolutionary contingency
Blount, Z. D. (2016) · Studies in History and Philosophy of Science Part C Studies in History and Philosophy of Biological and Biomedical Sciences · doi:10.1016/j.shpsc.2015.12.007 · Cited by 40 · see citing works
Lagomarsino, M. C., Espéli, O., & Junier, I. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.07.002 · Cited by 30 · see citing works
The landscape of transcriptional and translational changes over 22 years of bacterial adaptation
Favate, J. S., Liang, S., Cope, A. L., Yadavalli, S. S., & Shah, P. (2022) · eLife · doi:10.7554/elife.81979 · Cited by 28 · 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
Self-citationMaddamsetti, R., & Grant, N. A. (2020) · Genome Biology and Evolution · doi:10.1093/gbe/evaa178 · Cited by 29 · see citing works
Lamrabet, O., PLUMBRIDGE, J. A., Martin, M., Lenski, R. E., Schneider, D., & Hindré, T. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz042 · Cited by 25 · see citing works
Self-citationTransposable Prophage Mu Is Organized as a Stable Chromosomal Domain of E. coli
Saha, R. P., Lou, Z., Meng, L., & Harshey, R. M. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003902 · Cited by 24 · see citing works
Crozat, E., Hindré, T., Kühn, L., Garin, J., Lenski, R. E., & Schneider, D. (2010) · Journal of Bacteriology · doi:10.1128/jb.01341-10 · Cited by 21 · see citing works
Self-citationUpstream Binding of Idling RNA Polymerase Modulates Transcription Initiation from a Nearby Promoter
Gerganova, V., Maurer, S. P., Stoliar, L., Japaridze, A., Dietler, G., Nasser, W., Kutateladze, T. V., TRAVERS, A. A., & Muskhelishvili, G. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.628131 · Cited by 19 · see citing works
Zion, S., Katz, S., & Hershberg, R. (2024) · PLoS Genetics · doi:10.1371/journal.pgen.1011333 · Cited by 13 · see citing works
Puentes‐Téllez, P. E., Kovács, Á. T., Kuipers, O. P., & van Elsas, J. D. (2013) · Environmental Microbiology · doi:10.1111/1462-2920.12239 · Cited by 12 · see citing works
Baldridge, K. C., Jora, M., Maranhao, A. C., Quick, M. M., Addepalli, B., Brodbelt, J. S., Ellington, A. D., Limbach, P. A., & Contreras, L. M. (2018) · ACS Synthetic Biology · doi:10.1021/acssynbio.7b00421 · Cited by 12 · see citing works
Heyde, S. A. H., Frendorf, P. O., Lauritsen, I., & Nørholm, M. H. H. (2021) · mBio · doi:10.1128/mbio.02028-21 · Cited by 14 · see citing works
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Deatherage, D. E., & Barrick, J. E. (2021) · Cell Systems · doi:10.1016/j.cels.2021.08.011 · Cited by 10 · see citing works
The nucleoid as a smart polymer
Scolari, V. F., Sclavi, B., & Lagomarsino, M. C. (2015) · Frontiers in Microbiology · doi:10.3389/fmicb.2015.00424 · Cited by 10 · see citing works
The Evolution of Gene Regulatory Mechanisms in Bacteria
Dorman, C. J., Bhriain, N. N., & Dorman, M. J. (2018) · Grand challenges in biology and biotechnology · doi:10.1007/978-3-319-69078-0_6 · Cited by 11 · see citing works
Grohens, T., Meyer, S., & Beslon, G. (2025) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1013482 · Cited by 7 · see citing works
DNA topoisomerase I acts as supercoiling sensor for bacterial transcription elongation
Vidmar, V., Borde, C., Bruno, L., Miropolskaya, N., Takács, M., Batisse, C., Saint-André, C., Zhu, C., Espéli, O., Lamour, V., et al. (2025) · Nature Structural & Molecular Biology · doi:10.1038/s41594-025-01703-5 · Cited by 6 · see citing works
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A Genome-Wide Evolutionary Simulation of the Transcription-Supercoiling Coupling
Grohens, T., Meyer, S., & Beslon, G. (2022) · Artificial Life · doi:10.1162/artl_a_00373 · Cited by 5 · see citing works
On the study of evolutionary predictability using historical reconstructionPreprint
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Adaptive and pleiotropic effects of evolution in synonymous sugar environmentsPreprint
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DNA topoisomerase I acts as supercoiling sensor for transcription elongation in E. coliPreprint
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Chromatin is dispensable for bacterial lifePreprint
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Transposable prophage Mu exists as an independent chromosomal domain in E. coli
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Natural genetic engineering: intelligence & design in evolution?
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Testing the Major Theories Concerning the Evolution of Sex using Experimental Evolution
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Adaptation and diversification of Escherichia coli K12 MC1000 in a complex environment
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Evolution Underway in Prokaryotes
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- Authors
- Crozat, E., Winkworth, C., Gaffe, J., Hallin, P. F., Riley, M. A., Lenski, R. E., & Schneider, D.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Technical University of Denmark (DK)
- Michigan State University (US)
- Corresponding author
- Schneider, D.
- Venue
- Molecular Biology and Evolution
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-04-14
- Volume
- 27
- Issue
- 9
- Pages
- 2113-2128
- ISSN
- 0737-4038 (ISSN-L)
- 1537-1719
- OpenAlex
- W2167365021
- Cited by
- 62
- References
- 103
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 5 · 2023: 1 · 2022: 3 · 2021: 4 · 2020: 5 · 2019: 1 · 2018: 3 · 2017: 4 · 2016: 2 · 2015: 6 · 2014: 2 · 2013: 6 · 2012: 9
- FWCI
- 3.95
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Molecular Biology and Evolution (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Technical University of Denmark, DTU Orbit (Technical University of Denmark, DTU) (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-08-GENM-0023)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- DNA supercoiling, DNA superhelicity, parallel evolution, Escherichia coli, topA, topoisomerase I, FIS, positive selection, fitness effects of mutations, gene expression regulation, operon regulation, experimental evolution, chromosome structure
- MeSH terms
- DNA, Superhelical, Escherichia coli, Phenotype, Evolution, Molecular
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