2017
Maddamsetti R; Hatcher P J; Green A G; Williams B L; Marks D S; Lenski R E
Core genes evolve rapidly in the long-term evolution experiment with Escherichia coli Journal Article
Genome Biology and Evolution, 9 (4), pp. 1072–1083, 2017, ISSN: 17596653.
Abstract | Links | BibTeX | Altmetric | Tags: Genome Evolution, Genotypes and Phenotypes, Mutation Rates
@article{Maddamsetti2017,
title = {Core genes evolve rapidly in the long-term evolution experiment with \textit{Escherichia coli}},
author = {Rohan Maddamsetti and Philip J. Hatcher and Anna G. Green and Barry L. Williams and Debora S. Marks and Richard E. Lenski},
url = {https://academic.oup.com/gbe/article/9/4/1072/3100447},
doi = {10.1093/gbe/evx064},
issn = {17596653},
year = {2017},
date = {2017-01-01},
urldate = {2017-01-01},
journal = {Genome Biology and Evolution},
volume = {9},
number = {4},
pages = {1072--1083},
abstract = {Bacteria can evolve rapidly under positive selection owing to their vast numbers, allowing their genes to diversify by adapting to different environments. We asked whether the same genes that evolve rapidly in the long-term evolution experiment (LTEE) with \textit{Escherichia coli} have also diversified extensively in nature. To make this comparison, we identified ~2000 core genes shared among 60 \textit{E. coli} strains. During the LTEE, core genes accumulated significantly more nonsynonymous mutations than flexible (i.e., noncore) genes. Furthermore, core genes under positive selection in the LTEE are more conserved in nature than the average core gene. In some cases, adaptive mutations appear to modify protein functions, rather than merely knocking them out. The LTEE conditions are novel for \textit{E. coli}, at least in relation to its evolutionary history in nature. The constancy and simplicity of the environment likely favor the complete loss of some unused functions and the fine-tuning of others.},
keywords = {Genome Evolution, Genotypes and Phenotypes, Mutation Rates},
pubstate = {published},
tppubtype = {article}
}
Bacteria can evolve rapidly under positive selection owing to their vast numbers, allowing their genes to diversify by adapting to different environments. We asked whether the same genes that evolve rapidly in the long-term evolution experiment (LTEE) with Escherichia coli have also diversified extensively in nature. To make this comparison, we identified ~2000 core genes shared among 60 E. coli strains. During the LTEE, core genes accumulated significantly more nonsynonymous mutations than flexible (i.e., noncore) genes. Furthermore, core genes under positive selection in the LTEE are more conserved in nature than the average core gene. In some cases, adaptive mutations appear to modify protein functions, rather than merely knocking them out. The LTEE conditions are novel for E. coli, at least in relation to its evolutionary history in nature. The constancy and simplicity of the environment likely favor the complete loss of some unused functions and the fine-tuning of others.
2016
Großkopf T; Consuegra J; Gaffé J; Willison J C; Lenski R E; Soyer O S; Schneider D
Metabolic modelling in a dynamic evolutionary framework predicts adaptive diversification of bacteria in a long-term evolution experiment Journal Article
BMC Evolutionary Biology, 16 (1), pp. 163, 2016, ISSN: 1471-2148.
Abstract | Links | BibTeX | Altmetric | Tags: Demography and Ecology, Theory and Simulations
@article{Großkopf2016,
title = {Metabolic modelling in a dynamic evolutionary framework predicts adaptive diversification of bacteria in a long-term evolution experiment},
author = {Tobias Großkopf and Jessika Consuegra and Joël Gaffé and John C. Willison and Richard E. Lenski and Orkun S. Soyer and Dominique Schneider},
url = {https://bmcevolbiol.biomedcentral.com/articles/10.1186/s12862-016-0733-x},
doi = {10.1186/s12862-016-0733-x},
issn = {1471-2148},
year = {2016},
date = {2016-12-01},
urldate = {2016-12-01},
journal = {BMC Evolutionary Biology},
volume = {16},
number = {1},
pages = {163},
publisher = {BMC Evolutionary Biology},
abstract = {Background
Predicting adaptive trajectories is a major goal of evolutionary biology and useful for practical applications. Systems biology has enabled the development of genome-scale metabolic models. However, analysing these models via flux balance analysis (FBA) cannot predict many evolutionary outcomes including adaptive diversification, whereby an ancestral lineage diverges to fill multiple niches. Here we combine in silico evolution with FBA and apply this modelling framework, evoFBA, to a long-term evolution experiment with \textit{Escherichia coli}.
Results
Simulations predicted the adaptive diversification that occurred in one experimental population and generated hypotheses about the mechanisms that promoted coexistence of the diverged lineages. We experimentally tested and, on balance, verified these mechanisms, showing that diversification involved niche construction and character displacement through differential nutrient uptake and altered metabolic regulation.
Conclusion
The evoFBA framework represents a promising new way to model biochemical evolution, one that can generate testable predictions about evolutionary and ecosystem-level outcomes.},
keywords = {Demography and Ecology, Theory and Simulations},
pubstate = {published},
tppubtype = {article}
}
Background
Predicting adaptive trajectories is a major goal of evolutionary biology and useful for practical applications. Systems biology has enabled the development of genome-scale metabolic models. However, analysing these models via flux balance analysis (FBA) cannot predict many evolutionary outcomes including adaptive diversification, whereby an ancestral lineage diverges to fill multiple niches. Here we combine in silico evolution with FBA and apply this modelling framework, evoFBA, to a long-term evolution experiment with Escherichia coli.
Results
Simulations predicted the adaptive diversification that occurred in one experimental population and generated hypotheses about the mechanisms that promoted coexistence of the diverged lineages. We experimentally tested and, on balance, verified these mechanisms, showing that diversification involved niche construction and character displacement through differential nutrient uptake and altered metabolic regulation.
Conclusion
The evoFBA framework represents a promising new way to model biochemical evolution, one that can generate testable predictions about evolutionary and ecosystem-level outcomes.
Predicting adaptive trajectories is a major goal of evolutionary biology and useful for practical applications. Systems biology has enabled the development of genome-scale metabolic models. However, analysing these models via flux balance analysis (FBA) cannot predict many evolutionary outcomes including adaptive diversification, whereby an ancestral lineage diverges to fill multiple niches. Here we combine in silico evolution with FBA and apply this modelling framework, evoFBA, to a long-term evolution experiment with Escherichia coli.
Results
Simulations predicted the adaptive diversification that occurred in one experimental population and generated hypotheses about the mechanisms that promoted coexistence of the diverged lineages. We experimentally tested and, on balance, verified these mechanisms, showing that diversification involved niche construction and character displacement through differential nutrient uptake and altered metabolic regulation.
Conclusion
The evoFBA framework represents a promising new way to model biochemical evolution, one that can generate testable predictions about evolutionary and ecosystem-level outcomes.
Tenaillon O; Barrick J E; Ribeck N; Deatherage D E; Blanchard J L; Dasgupta A; Wu G C; Wielgoss S; Cruveiller S; Medigue C; Schneider D; Lenski R E
Tempo and mode of genome evolution in a 50,000-generation experiment. Journal Article
Nature, 536 (7615), pp. 165–170, 2016, ISSN: 1476-4687.
Abstract | Links | BibTeX | Altmetric | Tags: Genome Evolution, Mutation Rates, Parallelism and Divergence
@article{Tenaillon2016,
title = {Tempo and mode of genome evolution in a 50,000-generation experiment.},
author = {Olivier Tenaillon and Jeffrey E. Barrick and Noah Ribeck and Daniel E. Deatherage and Jeffrey L. Blanchard and Aurko Dasgupta and Gabriel C. Wu and Sebastien Wielgoss and Stephane Cruveiller and Claudine Medigue and Dominique Schneider and Richard E. Lenski},
url = {http://www.ncbi.nlm.nih.gov/pubmed/27479321},
doi = {10.1038/nature18959},
issn = {1476-4687},
year = {2016},
date = {2016-08-01},
urldate = {2016-08-01},
journal = {Nature},
volume = {536},
number = {7615},
pages = {165--170},
publisher = {Nature Publishing Group},
abstract = {Adaptation by natural selection depends on the rates, effects and interactions of many mutations, making it difficult to determine what proportion of mutations in an evolving lineage are beneficial. Here we analysed 264 complete genomes from 12 \textit{Escherichia coli} populations to characterize their dynamics over 50,000 generations. The populations that retained the ancestral mutation rate support a model in which most fixed mutations are beneficial, the fraction of beneficial mutations declines as fitness rises, and neutral mutations accumulate at a constant rate. We also compared these populations to mutation-accumulation lines evolved under a bottlenecking regime that minimizes selection. Nonsynonymous mutations, intergenic mutations, insertions and deletions are overrepresented in the long-term populations, further supporting the inference that most mutations that reached high frequency were favoured by selection. These results illuminate the shifting balance of forces that govern genome evolution in populations adapting to a new environment.},
keywords = {Genome Evolution, Mutation Rates, Parallelism and Divergence},
pubstate = {published},
tppubtype = {article}
}
Adaptation by natural selection depends on the rates, effects and interactions of many mutations, making it difficult to determine what proportion of mutations in an evolving lineage are beneficial. Here we analysed 264 complete genomes from 12 Escherichia coli populations to characterize their dynamics over 50,000 generations. The populations that retained the ancestral mutation rate support a model in which most fixed mutations are beneficial, the fraction of beneficial mutations declines as fitness rises, and neutral mutations accumulate at a constant rate. We also compared these populations to mutation-accumulation lines evolved under a bottlenecking regime that minimizes selection. Nonsynonymous mutations, intergenic mutations, insertions and deletions are overrepresented in the long-term populations, further supporting the inference that most mutations that reached high frequency were favoured by selection. These results illuminate the shifting balance of forces that govern genome evolution in populations adapting to a new environment.
Blount Z D
A case study in evolutionary contingency Journal Article
Studies in History and Philosophy of Science Part C: Studies in History and Philosophy of Biological and Biomedical Sciences, 58 , pp. 82–92, 2016, ISSN: 13698486.
Abstract | Links | BibTeX | Altmetric | Tags: Review Articles
@article{Blount2016,
title = {A case study in evolutionary contingency},
author = {Zachary D. Blount},
url = {https://linkinghub.elsevier.com/retrieve/pii/S1369848615001806},
doi = {10.1016/j.shpsc.2015.12.007},
issn = {13698486},
year = {2016},
date = {2016-08-01},
urldate = {2016-08-01},
journal = {Studies in History and Philosophy of Science Part C: Studies in History and Philosophy of Biological and Biomedical Sciences},
volume = {58},
pages = {82--92},
publisher = {Elsevier Ltd},
abstract = {Biological evolution is a fundamentally historical phenomenon in which intertwined stochastic and deterministic processes shape lineages with long, continuous histories that exist in a changing world that has a history of its own. The degree to which these characteristics render evolution historically contingent, and evolutionary outcomes thereby unpredictably sensitive to history has been the subject of considerable debate in recent decades. Microbial evolution experiments have proven among the most fruitful means of empirically investigating the issue of historical contingency in evolution. One such experiment is the \textit{Escherichia coli} Long-Term Evolution Experiment (LTEE), in which twelve populations founded from the same clone of \textit{E. coli} have evolved in parallel under identical conditions. Aerobic growth on citrate (Cit+), a novel trait for \textit{E. coli}, evolved in one of these populations after more than 30,000 generations. Experimental replays of this population's evolution from various points in its history showed that the Cit+ trait was historically contingent upon earlier mutations that potentiated the trait by rendering it mutationally accessible. Here I review this case of evolutionary contingency and discuss what it implies about the importance of historical contingency arising from the core processes of evolution.},
keywords = {Review Articles},
pubstate = {published},
tppubtype = {article}
}
Biological evolution is a fundamentally historical phenomenon in which intertwined stochastic and deterministic processes shape lineages with long, continuous histories that exist in a changing world that has a history of its own. The degree to which these characteristics render evolution historically contingent, and evolutionary outcomes thereby unpredictably sensitive to history has been the subject of considerable debate in recent decades. Microbial evolution experiments have proven among the most fruitful means of empirically investigating the issue of historical contingency in evolution. One such experiment is the Escherichia coli Long-Term Evolution Experiment (LTEE), in which twelve populations founded from the same clone of E. coli have evolved in parallel under identical conditions. Aerobic growth on citrate (Cit+), a novel trait for E. coli, evolved in one of these populations after more than 30,000 generations. Experimental replays of this population's evolution from various points in its history showed that the Cit+ trait was historically contingent upon earlier mutations that potentiated the trait by rendering it mutationally accessible. Here I review this case of evolutionary contingency and discuss what it implies about the importance of historical contingency arising from the core processes of evolution.
Ribeck N; Mulka J S; Zaman L; Connelly B D; Lenski R E
Competition between continuously evolving lineages in asexual populations Journal Article
bioRxiv, 2016.
Abstract | Links | BibTeX | Altmetric | Tags: Theory and Simulations
@article{Ribeck062976,
title = {Competition between continuously evolving lineages in asexual populations},
author = {Noah Ribeck and Joseph S. Mulka and Luis Zaman and Brian D. Connelly and Richard E. Lenski},
url = {https://www.biorxiv.org/content/early/2016/07/10/062976},
doi = {10.1101/062976},
year = {2016},
date = {2016-01-01},
urldate = {2016-01-01},
journal = {bioRxiv},
publisher = {Cold Spring Harbor Laboratory},
abstract = {In an asexual population, the fate of a beneficial mutation depends on how its lineage competes against other mutant lineages in the population. With high beneficial mutation rates or large population sizes, competition between contending mutations is strong, and successful lineages can accumulate multiple mutations before any single one achieves fixation. Most current theory about asexual population dynamics either neglects this multiple-mutations regime or introduces simplifying assumptions that may not apply. Here, we develop a theoretical framework that describes the dynamics of adaptation and substitution over all mutation-rate regimes by conceptualizing the population as a collection of continuously adapting lineages. This model of textquotedblleftlineage interferencetextquotedblright shows that each new mutanttextquoterights advantage over the rest of the population must be above a critical threshold in order to likely achieve fixation, and we derive a simple expression for that threshold. We apply this framework to examine the role of beneficial mutations with different effect sizes across the transition to the multiple-mutations regime.},
keywords = {Theory and Simulations},
pubstate = {published},
tppubtype = {article}
}
In an asexual population, the fate of a beneficial mutation depends on how its lineage competes against other mutant lineages in the population. With high beneficial mutation rates or large population sizes, competition between contending mutations is strong, and successful lineages can accumulate multiple mutations before any single one achieves fixation. Most current theory about asexual population dynamics either neglects this multiple-mutations regime or introduces simplifying assumptions that may not apply. Here, we develop a theoretical framework that describes the dynamics of adaptation and substitution over all mutation-rate regimes by conceptualizing the population as a collection of continuously adapting lineages. This model of textquotedblleftlineage interferencetextquotedblright shows that each new mutanttextquoterights advantage over the rest of the population must be above a critical threshold in order to likely achieve fixation, and we derive a simple expression for that threshold. We apply this framework to examine the role of beneficial mutations with different effect sizes across the transition to the multiple-mutations regime.
2015
Lenski R E; Wiser M J; Ribeck N; Blount Z D; Nahum J R; Morris J J; Zaman L; Turner C B; Wade B D; Maddamsetti R; Burmeister A R; Baird E J; Bundy J; Grant N A; Card K J; Rowles M; Weatherspoon K; Papoulis S E; Sullivan R; Clark C; Mulka J S; Hajela N
Sustained fitness gains and variability in fitness trajectories in the long-term evolution experiment with Escherichia coli Journal Article
Proceedings of the Royal Society B: Biological Sciences, 282 (1821), pp. 20152292, 2015, ISSN: 0962-8452.
Abstract | Links | BibTeX | Altmetric | Tags: Fitness Trajectories, Mutation Rates, Parallelism and Divergence
@article{nokey,
title = {Sustained fitness gains and variability in fitness trajectories in the long-term evolution experiment with \textit{Escherichia coli}},
author = {Richard E. Lenski and Michael J. Wiser and Noah Ribeck and Zachary D. Blount and Joshua R. Nahum and J. Jeffrey Morris and Luis Zaman and Caroline B. Turner and Brian D. Wade and Rohan Maddamsetti and Alita R. Burmeister and Elizabeth J. Baird and Jay Bundy and Nkrumah A. Grant and Kyle J. Card and Maia Rowles and Kiyana Weatherspoon and Spiridon E. Papoulis and Rachel Sullivan and Colleen Clark and Joseph S. Mulka and Neerja Hajela},
url = {https://royalsocietypublishing.org/doi/10.1098/rspb.2015.2292},
doi = {10.1098/rspb.2015.2292},
issn = {0962-8452},
year = {2015},
date = {2015-12-22},
urldate = {2015-12-22},
journal = {Proceedings of the Royal Society B: Biological Sciences},
volume = {282},
number = {1821},
pages = {20152292},
abstract = {Many populations live in environments subject to frequent biotic and abiotic changes. Nonetheless, it is interesting to ask whether an evolving population's mean fitness can increase indefinitely, and potentially without any limit, even in a constant environment. A recent study showed that fitness trajectories of \textit{Escherichia coli} populations over 50 000 generations were better described by a power-law model than by a hyperbolic model. According to the power-law model, the rate of fitness gain declines over time but fitness has no upper limit, whereas the hyperbolic model implies a hard limit. Here, we examine whether the previously estimated power-law model predicts the fitness trajectory for an additional 10 000 generations. To that end, we conducted more than 1100 new competitive fitness assays. Consistent with the previous study, the power-law model fits the new data better than the hyperbolic model. We also analysed the variability in fitness among populations, finding subtle, but significant, heterogeneity in mean fitness. Some, but not all, of this variation reflects differences in mutation rate that evolved over time. Taken together, our results imply that both adaptation and divergence can continue indefinitely—or at least for a long time—even in a constant environment.},
keywords = {Fitness Trajectories, Mutation Rates, Parallelism and Divergence},
pubstate = {published},
tppubtype = {article}
}
Many populations live in environments subject to frequent biotic and abiotic changes. Nonetheless, it is interesting to ask whether an evolving population's mean fitness can increase indefinitely, and potentially without any limit, even in a constant environment. A recent study showed that fitness trajectories of Escherichia coli populations over 50 000 generations were better described by a power-law model than by a hyperbolic model. According to the power-law model, the rate of fitness gain declines over time but fitness has no upper limit, whereas the hyperbolic model implies a hard limit. Here, we examine whether the previously estimated power-law model predicts the fitness trajectory for an additional 10 000 generations. To that end, we conducted more than 1100 new competitive fitness assays. Consistent with the previous study, the power-law model fits the new data better than the hyperbolic model. We also analysed the variability in fitness among populations, finding subtle, but significant, heterogeneity in mean fitness. Some, but not all, of this variation reflects differences in mutation rate that evolved over time. Taken together, our results imply that both adaptation and divergence can continue indefinitely—or at least for a long time—even in a constant environment.
Maddamsetti R; Hatcher P J; Cruveiller S; Medigue C; Barrick J E; Lenski R E
Molecular Biology and Evolution, 32 (11), 2015, ISSN: 0737-4038.
Abstract | Links | BibTeX | Altmetric | Tags: Genome Evolution
@article{Maddamsetti2015,
title = {Synonymous Genetic Variation in Natural Isolates of \textit{Escherichia coli} Does Not Predict Where Synonymous Substitutions Occur in a Long-Term Experiment},
author = {Rohan Maddamsetti and Philip J. Hatcher and Stephane Cruveiller and Claudine Medigue and Jeffrey E. Barrick and Richard E. Lenski},
url = {https://academic.oup.com/mbe/article-lookup/doi/10.1093/molbev/msv161},
doi = {10.1093/molbev/msv161},
issn = {0737-4038},
year = {2015},
date = {2015-11-01},
urldate = {2015-11-01},
journal = {Molecular Biology and Evolution},
volume = {32},
number = {11},
abstract = {Synonymous genetic differences vary by more than 20-fold among genes in natural isolates of \textit{Escherichia coli}. One hypothesis to explain this heterogeneity is that genes with high levels of synonymous variation mutate at higher rates than genes with low synonymous variation. If so, then one would expect to observe similar mutational patterns in evolution experiments. In fact, however, the pattern of synonymous substitutions in a long-term evolution experiment with \textit{E. coli} does not support this hypothesis. In particular, the extent of synonymous variation across genes in that experiment does not reflect the variation observed in natural isolates of \textit{E. coli}. Instead, gene length alone predicts with high accuracy the prevalence of synonymous changes in the experimental populations. We hypothesize that patterns of synonymous variation in natural \textit{E. coli} populations are instead caused by differences across genomic regions in their effective population size that, in turn, reflect different histories of recombination, horizontal gene transfer, selection, and population structure.},
keywords = {Genome Evolution},
pubstate = {published},
tppubtype = {article}
}
Synonymous genetic differences vary by more than 20-fold among genes in natural isolates of Escherichia coli. One hypothesis to explain this heterogeneity is that genes with high levels of synonymous variation mutate at higher rates than genes with low synonymous variation. If so, then one would expect to observe similar mutational patterns in evolution experiments. In fact, however, the pattern of synonymous substitutions in a long-term evolution experiment with E. coli does not support this hypothesis. In particular, the extent of synonymous variation across genes in that experiment does not reflect the variation observed in natural isolates of E. coli. Instead, gene length alone predicts with high accuracy the prevalence of synonymous changes in the experimental populations. We hypothesize that patterns of synonymous variation in natural E. coli populations are instead caused by differences across genomic regions in their effective population size that, in turn, reflect different histories of recombination, horizontal gene transfer, selection, and population structure.
Turner C B; Blount Z D; Lenski R E
Replaying Evolution to Test the Cause of Extinction of One Ecotype in an Experimentally Evolved Population Journal Article
PLOS ONE, 10 (11), pp. e0142050, 2015, ISSN: 1932-6203.
Abstract | Links | BibTeX | Altmetric | Tags: Citrate Evolution, Demography and Ecology, Historical Contingency
@article{Turner2015,
title = {Replaying Evolution to Test the Cause of Extinction of One Ecotype in an Experimentally Evolved Population},
author = {Caroline B. Turner and Zachary D. Blount and Richard E. Lenski},
editor = {Frederick M. Cohan},
url = {https://dx.plos.org/10.1371/journal.pone.0142050},
doi = {10.1371/journal.pone.0142050},
issn = {1932-6203},
year = {2015},
date = {2015-11-01},
urldate = {2015-11-01},
journal = {PLOS ONE},
volume = {10},
number = {11},
pages = {e0142050},
abstract = {In a long-term evolution experiment with \textit{Escherichia coli}, bacteria in one of twelve populations evolved the ability to consume citrate, a previously unexploited resource in a glucoselimited medium. This innovation led to the frequency-dependent coexistence of citrate-consuming (Cit+) and non-consuming (Cit-) ecotypes, with Cit-bacteria persisting on the exogenously supplied glucose as well as other carbon molecules released by the Cit+ bacteria. After more than 10,000 generations of coexistence, however, the Cit-lineage went extinct; cells with the Cit-phenotype dropped to levels below detection, and the Cit-clade could not be detected by molecular assays based on its unique genotype. We hypothesized that this extinction was a deterministic outcome of evolutionary change within the population, specifically the appearance of a more-fit Cit+ ecotype that competitively excluded the Cit-ecotype. We tested this hypothesis by re-evolving the population from a frozen population sample taken within 500 generations of the extinction and from another sample taken several thousand generations earlier, in each case for 500 generations and with 20-fold replication. To our surprise, the Cit-type did not go extinct in any of these replays, and Cit-cells also persisted in a single replicate that was propagated for 2,500 generations. Even more unexpectedly, we showed that the Cit-ecotype could reinvade the Cit+ population after its extinction. Taken together, these results indicate that the extinction of the Cit-ecotype was not a deterministic outcome driven by competitive exclusion by the Cit+ ecotype. The extinction also cannot be explained by demographic stochasticity alone, as the population size of the Cit-ecotype should have been many thousands of cells even during the daily transfer events. Instead, we infer that the extinction must have been caused by a rare chance event in which some aspect of the experimental conditions was inadvertently perturbed.},
keywords = {Citrate Evolution, Demography and Ecology, Historical Contingency},
pubstate = {published},
tppubtype = {article}
}
In a long-term evolution experiment with Escherichia coli, bacteria in one of twelve populations evolved the ability to consume citrate, a previously unexploited resource in a glucoselimited medium. This innovation led to the frequency-dependent coexistence of citrate-consuming (Cit+) and non-consuming (Cit-) ecotypes, with Cit-bacteria persisting on the exogenously supplied glucose as well as other carbon molecules released by the Cit+ bacteria. After more than 10,000 generations of coexistence, however, the Cit-lineage went extinct; cells with the Cit-phenotype dropped to levels below detection, and the Cit-clade could not be detected by molecular assays based on its unique genotype. We hypothesized that this extinction was a deterministic outcome of evolutionary change within the population, specifically the appearance of a more-fit Cit+ ecotype that competitively excluded the Cit-ecotype. We tested this hypothesis by re-evolving the population from a frozen population sample taken within 500 generations of the extinction and from another sample taken several thousand generations earlier, in each case for 500 generations and with 20-fold replication. To our surprise, the Cit-type did not go extinct in any of these replays, and Cit-cells also persisted in a single replicate that was propagated for 2,500 generations. Even more unexpectedly, we showed that the Cit-ecotype could reinvade the Cit+ population after its extinction. Taken together, these results indicate that the extinction of the Cit-ecotype was not a deterministic outcome driven by competitive exclusion by the Cit+ ecotype. The extinction also cannot be explained by demographic stochasticity alone, as the population size of the Cit-ecotype should have been many thousands of cells even during the daily transfer events. Instead, we infer that the extinction must have been caused by a rare chance event in which some aspect of the experimental conditions was inadvertently perturbed.
Quandt E M; Gollihar J; Blount Z D; Ellington A D; Georgiou G; Barrick J E
Fine-tuning citrate synthase flux potentiates and refines metabolic innovation in the Lenski evolution experiment. Journal Article
eLife, 4 (October), pp. e09696, 2015, ISSN: 2050-084X.
Abstract | Links | BibTeX | Altmetric | Tags: Citrate Evolution, Genotypes and Phenotypes, Historical Contingency
@article{Quandt2015,
title = {Fine-tuning citrate synthase flux potentiates and refines metabolic innovation in the Lenski evolution experiment.},
author = {Erik M. Quandt and Jimmy Gollihar and Zachary D. Blount and Andrew D. Ellington and George Georgiou and Jeffrey E. Barrick},
url = {http://www.ncbi.nlm.nih.gov/pubmed/26465114
http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=PMC4718724},
doi = {10.7554/eLife.09696},
issn = {2050-084X},
year = {2015},
date = {2015-10-01},
urldate = {2015-10-01},
journal = {eLife},
volume = {4},
number = {October},
pages = {e09696},
abstract = {Evolutionary innovations that enable organisms to colonize new ecological niches are rare compared to gradual evolutionary changes in existing traits. We discovered that key mutations in the \textit{gltA} gene, which encodes citrate synthase (CS), occurred both before and after \textit{Escherichia coli} gained the ability to grow aerobically on citrate (Cit(+) phenotype) during the Lenski long-term evolution experiment. The first \textit{gltA} mutation, which increases CS activity by disrupting NADH-inhibition of this enzyme, is beneficial for growth on the acetate and contributed to preserving the rudimentary Cit(+) trait from extinction when it first evolved. However, after Cit(+) was refined by further mutations, this potentiating \textit{gltA} mutation became deleterious to fitness. A second wave of beneficial \textit{gltA} mutations then evolved that reduced CS activity to below the ancestral level. Thus, dynamic reorganization of central metabolism made colonizing this new nutrient niche contingent on both co-opting and overcoming a history of prior adaptation.},
keywords = {Citrate Evolution, Genotypes and Phenotypes, Historical Contingency},
pubstate = {published},
tppubtype = {article}
}
Evolutionary innovations that enable organisms to colonize new ecological niches are rare compared to gradual evolutionary changes in existing traits. We discovered that key mutations in the gltA gene, which encodes citrate synthase (CS), occurred both before and after Escherichia coli gained the ability to grow aerobically on citrate (Cit(+) phenotype) during the Lenski long-term evolution experiment. The first gltA mutation, which increases CS activity by disrupting NADH-inhibition of this enzyme, is beneficial for growth on the acetate and contributed to preserving the rudimentary Cit(+) trait from extinction when it first evolved. However, after Cit(+) was refined by further mutations, this potentiating gltA mutation became deleterious to fitness. A second wave of beneficial gltA mutations then evolved that reduced CS activity to below the ancestral level. Thus, dynamic reorganization of central metabolism made colonizing this new nutrient niche contingent on both co-opting and overcoming a history of prior adaptation.
Satterwhite R S; Cooper T F
Constraints on adaptation of Escherichia coli to mixed-resource environments increase over time Journal Article
Evolution, 69 (8), pp. 2067–2078, 2015, ISSN: 00143820.
Abstract | Links | BibTeX | Altmetric | Tags: Descendant Experiments
@article{Satterwhite2015,
title = {Constraints on adaptation of \textit{Escherichia coli} to mixed-resource environments increase over time},
author = {Rebecca S. Satterwhite and Tim F. Cooper},
url = {https://onlinelibrary.wiley.com/doi/10.1111/evo.12710},
doi = {10.1111/evo.12710},
issn = {00143820},
year = {2015},
date = {2015-08-01},
urldate = {2015-08-01},
journal = {Evolution},
volume = {69},
number = {8},
pages = {2067--2078},
abstract = {Can a population evolved in two resources reach the same fitness in both as specialist populations evolved in each of the individual resources? This question is central to theories of ecological specialization, the maintenance of genetic variation, and sympatric speciation, yet relatively few experiments have examined costs of generalism over long-term adaptation. We tested whether selection in environments containing two resources limits a population's ability to adapt to the individual resources by comparing the fitness of replicate \textit{Escherichia coli} populations evolved for 6000 generations in the presence of glucose or lactose alone (specialists), or in varying presentations of glucose and lactose together (generalists). We found that all populations had significant fitness increases in both resources, though the magnitude and rate of these increases differed. For the first 4000 generations, most generalist populations increased in fitness as quickly in the individual resources as the corresponding specialist populations. From 5000 generations, however, a widespread cost of adaptation affected all generalists, indicating a growing constraint on their abilities to adapt to two resources simultaneously. Our results indicate that costs of generalism are prevalent, but may influence evolutionary trajectories only after a period of cost-free adaptation.},
keywords = {Descendant Experiments},
pubstate = {published},
tppubtype = {article}
}
Can a population evolved in two resources reach the same fitness in both as specialist populations evolved in each of the individual resources? This question is central to theories of ecological specialization, the maintenance of genetic variation, and sympatric speciation, yet relatively few experiments have examined costs of generalism over long-term adaptation. We tested whether selection in environments containing two resources limits a population's ability to adapt to the individual resources by comparing the fitness of replicate Escherichia coli populations evolved for 6000 generations in the presence of glucose or lactose alone (specialists), or in varying presentations of glucose and lactose together (generalists). We found that all populations had significant fitness increases in both resources, though the magnitude and rate of these increases differed. For the first 4000 generations, most generalist populations increased in fitness as quickly in the individual resources as the corresponding specialist populations. From 5000 generations, however, a widespread cost of adaptation affected all generalists, indicating a growing constraint on their abilities to adapt to two resources simultaneously. Our results indicate that costs of generalism are prevalent, but may influence evolutionary trajectories only after a period of cost-free adaptation.
Fox J W; Lenski R E
From Here to Eternity—The Theory and Practice of a Really Long Experiment Journal Article
PLOS Biology, 13 (3), pp. e1002185, 2015, ISSN: 1545-7885.
Abstract | Links | BibTeX | Altmetric | Tags: Review Articles
@article{nokey,
title = {From Here to Eternity—The Theory and Practice of a Really Long Experiment},
author = {Jeremy W. Fox and Richard E. Lenski},
url = {https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.1002185},
doi = {10.1371/journal.pbio.1002185},
issn = {1545-7885},
year = {2015},
date = {2015-06-23},
urldate = {2015-06-23},
journal = {PLOS Biology},
volume = {13},
number = {3},
pages = { e1002185},
abstract = {In February 1988, Richard Lenski set up 12 replicate populations of a single genotype of \textit{Escherichia coli} in a simple nutrient medium. He has been following their evolution ever since. Here, Lenski answers provocative questions from Jeremy Fox about his iconic "Long-Term Evolution Experiment" (LTEE). The LTEE is a remarkable case study of the interplay of determinism and chance in evolution—and in the conduct of science.},
keywords = {Review Articles},
pubstate = {published},
tppubtype = {article}
}
In February 1988, Richard Lenski set up 12 replicate populations of a single genotype of Escherichia coli in a simple nutrient medium. He has been following their evolution ever since. Here, Lenski answers provocative questions from Jeremy Fox about his iconic "Long-Term Evolution Experiment" (LTEE). The LTEE is a remarkable case study of the interplay of determinism and chance in evolution—and in the conduct of science.
Turner C B; Blount Z D; Mitchell D; Lenski R E
bioRxiv, 2015.
Abstract | Links | BibTeX | Altmetric | Tags: Citrate Evolution, Demography and Ecology
@unpublished{nokey,
title = {Evolution and coexistence in response to a key innovation in a long-term evolution experiment with \textit{Escherichia coli}},
author = {Caroline B. Turner and Zachary D. Blount and Daniel Mitchell and Richard E. Lenski},
url = {https://www.biorxiv.org/content/10.1101/020958v1},
doi = {https://doi.org/10.1101/020958},
year = {2015},
date = {2015-06-17},
urldate = {2015-06-17},
journal = {bioRxiv},
abstract = {Evolution of a novel function can greatly alter the effects of an organism on its environment. These environmental changes can, in turn, affect the further evolution of that organism and any coexisting organisms. We examine these effects and feedbacks following evolution of a novel function in the long-term evolution experiment (LTEE) with \textit{Escherichia coli}. A characteristic feature of \textit{E. coli} is its inability to consume citrate aerobically. However, that ability evolved in one of the LTEE populations. In this population, citrate-utilizing bacteria (Cit+) coexisted stably with another clade of bacteria that lacked the capacity to utilize citrate (Cit−). This coexistence was shaped by the evolution of a cross-feeding relationship in which Cit+ cells released the dicarboxylic acids succinate, fumarate, and malate into the medium, and Cit− cells evolved improved growth on these carbon sources, as did the Cit+ cells. Thus, the evolution of citrate consumption led to a flask-based ecosystem that went from a single limiting resource, glucose, to one with five resources either shared or partitioned between two coexisting clades. Our findings show how evolutionary novelties can change environmental conditions, thereby facilitating diversity and altering both the structure of an ecosystem and the evolutionary trajectories of coexisting organisms.
\textit{Evolution does not produce novelties from scratch. It works on what already exists, either transforming a system to give it new functions or combining several systems to produce a more elaborate one.
–Francois Jacob}},
howpublished = {bioRxiv},
keywords = {Citrate Evolution, Demography and Ecology},
pubstate = {published},
tppubtype = {unpublished}
}
Evolution of a novel function can greatly alter the effects of an organism on its environment. These environmental changes can, in turn, affect the further evolution of that organism and any coexisting organisms. We examine these effects and feedbacks following evolution of a novel function in the long-term evolution experiment (LTEE) with Escherichia coli. A characteristic feature of E. coli is its inability to consume citrate aerobically. However, that ability evolved in one of the LTEE populations. In this population, citrate-utilizing bacteria (Cit+) coexisted stably with another clade of bacteria that lacked the capacity to utilize citrate (Cit−). This coexistence was shaped by the evolution of a cross-feeding relationship in which Cit+ cells released the dicarboxylic acids succinate, fumarate, and malate into the medium, and Cit− cells evolved improved growth on these carbon sources, as did the Cit+ cells. Thus, the evolution of citrate consumption led to a flask-based ecosystem that went from a single limiting resource, glucose, to one with five resources either shared or partitioned between two coexisting clades. Our findings show how evolutionary novelties can change environmental conditions, thereby facilitating diversity and altering both the structure of an ecosystem and the evolutionary trajectories of coexisting organisms.
Evolution does not produce novelties from scratch. It works on what already exists, either transforming a system to give it new functions or combining several systems to produce a more elaborate one.
–Francois Jacob
Evolution does not produce novelties from scratch. It works on what already exists, either transforming a system to give it new functions or combining several systems to produce a more elaborate one.
–Francois Jacob
Wiser M J; Lenski R E
A Comparison of Methods to Measure Fitness in Escherichia coli Journal Article
PLOS ONE, 10 (5), pp. e0126210, 2015, ISSN: 1932-6203.
Abstract | Links | BibTeX | Altmetric | Tags: Methods and Miscellaneous
@article{Wiser2015,
title = {A Comparison of Methods to Measure Fitness in \textit{Escherichia coli}},
author = {Michael J. Wiser and Richard E. Lenski},
editor = {Jeffrey L Blanchard},
url = {https://dx.plos.org/10.1371/journal.pone.0126210},
doi = {10.1371/journal.pone.0126210},
issn = {1932-6203},
year = {2015},
date = {2015-05-01},
urldate = {2015-05-01},
journal = {PLOS ONE},
volume = {10},
number = {5},
pages = {e0126210},
abstract = {In order to characterize the dynamics of adaptation, it is important to be able to quantify how a population's mean fitness changes over time. Such measurements are especially important in experimental studies of evolution using microbes. The Long-Term Evolution Experiment (LTEE) with \textit{Escherichia coli} provides one such system in which mean fitness has been measured by competing derived and ancestral populations. The traditional method used to measure fitness in the LTEE and many similar experiments, though, is subject to a potential limitation. As the relative fitness of the two competitors diverges, the measurement error increases because the less-fit population becomes increasingly small and cannot be enumerated as precisely. Here, we present and employ two alternatives to the traditional method. One is based on reducing the fitness differential between the competitors by using a common reference competitor from an intermediate generation that has intermediate fitness; the other alternative increases the initial population size of the less-fit, ancestral competitor. We performed a total of 480 competitions to compare the statistical properties of estimates obtained using these alternative methods with those obtained using the traditional method for samples taken over 50,000 generations from one of the LTEE populations. On balance, neither alternative method yielded measurements that were more precise than the traditional method.},
keywords = {Methods and Miscellaneous},
pubstate = {published},
tppubtype = {article}
}
In order to characterize the dynamics of adaptation, it is important to be able to quantify how a population's mean fitness changes over time. Such measurements are especially important in experimental studies of evolution using microbes. The Long-Term Evolution Experiment (LTEE) with Escherichia coli provides one such system in which mean fitness has been measured by competing derived and ancestral populations. The traditional method used to measure fitness in the LTEE and many similar experiments, though, is subject to a potential limitation. As the relative fitness of the two competitors diverges, the measurement error increases because the less-fit population becomes increasingly small and cannot be enumerated as precisely. Here, we present and employ two alternatives to the traditional method. One is based on reducing the fitness differential between the competitors by using a common reference competitor from an intermediate generation that has intermediate fitness; the other alternative increases the initial population size of the less-fit, ancestral competitor. We performed a total of 480 competitions to compare the statistical properties of estimates obtained using these alternative methods with those obtained using the traditional method for samples taken over 50,000 generations from one of the LTEE populations. On balance, neither alternative method yielded measurements that were more precise than the traditional method.
Ribeck N; Lenski R E
Modeling and quantifying frequency-dependent fitness in microbial populations with cross-feeding interactions Journal Article
Evolution, 69 (5), pp. 1313–1320, 2015, ISSN: 00143820.
Abstract | Links | BibTeX | Altmetric | Tags: Demography and Ecology, Theory and Simulations
@article{Ribeck2015,
title = {Modeling and quantifying frequency-dependent fitness in microbial populations with cross-feeding interactions},
author = {Noah Ribeck and Richard E. Lenski},
url = {https://onlinelibrary.wiley.com/doi/10.1111/evo.12645},
doi = {10.1111/evo.12645},
issn = {00143820},
year = {2015},
date = {2015-05-01},
urldate = {2015-05-01},
journal = {Evolution},
volume = {69},
number = {5},
pages = {1313--1320},
abstract = {Coexistence of two or more populations by frequency-dependent selection is common in nature, and it often arises even in well-mixed experiments with microbes. If ecology is to be incorporated into models of population genetics, then it is important to represent accurately the functional form of frequency-dependent interactions. However, measuring this functional form is problematic for traditional fitness assays, which assume a constant fitness difference between competitors over the course of an assay. Here, we present a theoretical framework for measuring the functional form of frequency-dependent fitness by accounting for changes in abundance and relative fitness during a competition assay. Using two examples of ecological coexistence that arose in a long-term evolution experiment with \textit{Escherichia coli}, we illustrate accurate quantification of the functional form of frequency-dependent relative fitness. Using a Monod-type model of growth dynamics, we show that two ecotypes in a typical cross-feeding interaction-such as when one bacterial population uses a byproduct generated by another-yields relative fitness that is linear with relative frequency.},
keywords = {Demography and Ecology, Theory and Simulations},
pubstate = {published},
tppubtype = {article}
}
Coexistence of two or more populations by frequency-dependent selection is common in nature, and it often arises even in well-mixed experiments with microbes. If ecology is to be incorporated into models of population genetics, then it is important to represent accurately the functional form of frequency-dependent interactions. However, measuring this functional form is problematic for traditional fitness assays, which assume a constant fitness difference between competitors over the course of an assay. Here, we present a theoretical framework for measuring the functional form of frequency-dependent fitness by accounting for changes in abundance and relative fitness during a competition assay. Using two examples of ecological coexistence that arose in a long-term evolution experiment with Escherichia coli, we illustrate accurate quantification of the functional form of frequency-dependent relative fitness. Using a Monod-type model of growth dynamics, we show that two ecotypes in a typical cross-feeding interaction-such as when one bacterial population uses a byproduct generated by another-yields relative fitness that is linear with relative frequency.
Maddamsetti R; Lenski R E; Barrick J E
Adaptation, Clonal Interference, and Frequency-Dependent Interactions in a Long-Term Evolution Experiment with Escherichia coli Journal Article
Genetics, 200 (2), pp. 619-631, 2015, ISSN: 1943-2631.
Abstract | Links | BibTeX | Altmetric | Tags: Demography and Ecology, Fitness Trajectories, Genome Evolution
@article{nokey,
title = {Adaptation, Clonal Interference, and Frequency-Dependent Interactions in a Long-Term Evolution Experiment with \emph{Escherichia coli}},
author = {Rohan Maddamsetti and Richard E. Lenski and Jeffrey E. Barrick},
url = {https://academic.oup.com/genetics/article/200/2/619/5936186},
doi = {10.1534/genetics.115.176677},
issn = {1943-2631},
year = {2015},
date = {2015-04-24},
urldate = {2015-04-24},
journal = {Genetics},
volume = {200},
number = {2},
pages = {619-631},
abstract = {Twelve replicate populations of \textit{Escherichia coli} have been evolving in the laboratory for >25 years and 60,000 generations. We analyzed bacteria from whole-population samples frozen every 500 generations through 20,000 generations for one well-studied population, called Ara−1. By tracking 42 known mutations in these samples, we reconstructed the history of this population’s genotypic evolution over this period. The evolutionary dynamics of Ara−1 show strong evidence of selective sweeps as well as clonal interference between competing lineages bearing different beneficial mutations. In some cases, sets of several mutations approached fixation simultaneously, often conveying no information about their order of origination; we present several possible explanations for the existence of these mutational cohorts. Against a backdrop of rapid selective sweeps both earlier and later, two genetically diverged clades coexisted for >6000 generations before one went extinct. In that time, many additional mutations arose in the clade that eventually prevailed. We show that the clades evolved a frequency-dependent interaction, which prevented the immediate competitive exclusion of either clade, but which collapsed as beneficial mutations accumulated in the clade that prevailed. Clonal interference and frequency dependence can occur even in the simplest microbial populations. Furthermore, frequency dependence may generate dynamics that extend the period of coexistence that would otherwise be sustained by clonal interference alone.},
keywords = {Demography and Ecology, Fitness Trajectories, Genome Evolution},
pubstate = {published},
tppubtype = {article}
}
Twelve replicate populations of Escherichia coli have been evolving in the laboratory for >25 years and 60,000 generations. We analyzed bacteria from whole-population samples frozen every 500 generations through 20,000 generations for one well-studied population, called Ara−1. By tracking 42 known mutations in these samples, we reconstructed the history of this population’s genotypic evolution over this period. The evolutionary dynamics of Ara−1 show strong evidence of selective sweeps as well as clonal interference between competing lineages bearing different beneficial mutations. In some cases, sets of several mutations approached fixation simultaneously, often conveying no information about their order of origination; we present several possible explanations for the existence of these mutational cohorts. Against a backdrop of rapid selective sweeps both earlier and later, two genetically diverged clades coexisted for >6000 generations before one went extinct. In that time, many additional mutations arose in the clade that eventually prevailed. We show that the clades evolved a frequency-dependent interaction, which prevented the immediate competitive exclusion of either clade, but which collapsed as beneficial mutations accumulated in the clade that prevailed. Clonal interference and frequency dependence can occur even in the simplest microbial populations. Furthermore, frequency dependence may generate dynamics that extend the period of coexistence that would otherwise be sustained by clonal interference alone.
Rudan M; Schneider D; Warnecke T; Krisko A
RNA chaperones buffer deleterious mutations in E. coli Journal Article
eLife, 4 , 2015, ISSN: 2050-084X.
Abstract | Links | BibTeX | Altmetric | Tags: Genotypes and Phenotypes
@article{Rudan2015,
title = {RNA chaperones buffer deleterious mutations in \textit{E. coli}},
author = {Marina Rudan and Dominique Schneider and Tobias Warnecke and Anita Krisko},
url = {https://elifesciences.org/articles/04745},
doi = {10.7554/eLife.04745},
issn = {2050-084X},
year = {2015},
date = {2015-03-01},
urldate = {2015-03-01},
journal = {eLife},
volume = {4},
abstract = {Both proteins and RNAs can misfold into non-functional conformations. Protein chaperones promote native folding of nascent polypeptides and refolding of misfolded species, thereby buffering mutations that compromise protein structure and function. Here, we show that RNA chaperones can also act as mutation buffers that enhance organismal fitness. Using competition assays, we demonstrate that overexpression of select RNA chaperones, including three DEAD box RNA helicases (DBRHs) (CsdA, SrmB, RhlB) and the cold shock protein CspA, improves fitness of two independently evolved \textit{Escherichia coli} mutator strains that have accumulated deleterious mutations during short- and long-term laboratory evolution. We identify strain-specific mutations that are deleterious and subject to buffering when introduced individually into the ancestral genotype. For DBRHs, we show that buffering requires helicase activity, implicating RNA structural remodelling in the buffering process. Our results suggest that RNA chaperones might play a fundamental role in RNA evolution and evolvability.},
keywords = {Genotypes and Phenotypes},
pubstate = {published},
tppubtype = {article}
}
Both proteins and RNAs can misfold into non-functional conformations. Protein chaperones promote native folding of nascent polypeptides and refolding of misfolded species, thereby buffering mutations that compromise protein structure and function. Here, we show that RNA chaperones can also act as mutation buffers that enhance organismal fitness. Using competition assays, we demonstrate that overexpression of select RNA chaperones, including three DEAD box RNA helicases (DBRHs) (CsdA, SrmB, RhlB) and the cold shock protein CspA, improves fitness of two independently evolved Escherichia coli mutator strains that have accumulated deleterious mutations during short- and long-term laboratory evolution. We identify strain-specific mutations that are deleterious and subject to buffering when introduced individually into the ancestral genotype. For DBRHs, we show that buffering requires helicase activity, implicating RNA structural remodelling in the buffering process. Our results suggest that RNA chaperones might play a fundamental role in RNA evolution and evolvability.
2014
Raeside C; Gaffé J; Deatherage D E; Tenaillon O; Briska A M; Ptashkin R N; Cruveiller S; Médigue C; Lenski R E; Barrick J E; Schneider D
Large Chromosomal Rearrangements during a Long-Term Evolution Experiment with Escherichia coli Journal Article
mBio, 5 (5), pp. 1–13, 2014, ISSN: 2161-2129.
Abstract | Links | BibTeX | Altmetric | Tags: Genome Evolution
@article{Raeside2014,
title = {Large Chromosomal Rearrangements during a Long-Term Evolution Experiment with \textit{Escherichia coli}},
author = {Colin Raeside and Joël Gaffé and Daniel E. Deatherage and Olivier Tenaillon and Adam M. Briska and Ryan N. Ptashkin and Stéphane Cruveiller and Claudine Médigue and Richard E. Lenski and Jeffrey E. Barrick and Dominique Schneider},
editor = {Søren Molin and Fernando Baquero},
url = {https://journals.asm.org/doi/10.1128/mBio.01377-14},
doi = {10.1128/mBio.01377-14},
issn = {2161-2129},
year = {2014},
date = {2014-10-01},
urldate = {2014-10-01},
journal = {mBio},
volume = {5},
number = {5},
pages = {1--13},
abstract = {Large-scale rearrangements may be important in evolution because they can alter chromosome organization and gene expression in ways not possible through point mutations. In a long-term evolution experiment, twelve \textit{Escherichia coli} populations have been propagated in a glucose-limited environment for over 25 years. We used whole-genome mapping (optical mapping) combined with genome sequencing and PCR analysis to identify the large-scale chromosomal rearrangements in clones from each population after 40,000 generations. A total of 110 rearrangement events were detected, including 82 deletions, 19 inversions, and 9 duplications, with lineages having between 5 and 20 events. In three populations, successive rearrangements impacted particular regions. In five populations, rearrangements affected over a third of the chromosome. Most rearrangements involved recombination between insertion sequence (IS) elements, illustrating their importance in mediating genome plasticity. Two lines of evidence suggest that at least some of these rearrangements conferred higher fitness. First, parallel changes were observed across the independent populations, with ~65% of the rearrangements affecting the same loci in at least two populations. For example, the ribose-utilization operon and the \textit{manB} - \textit{cpsG} region were deleted in 12 and 10 populations, respectively, suggesting positive selection, and this inference was previously confirmed for the former case. Second, optical maps from clones sampled over time from one population showed that most rearrangements occurred early in the experiment, when fitness was increasing most rapidly. However, some rearrangements likely occur at high frequency and may have simply hitchhiked to fixation. In any case, large-scale rearrangements clearly influenced genomic evolution in these populations.},
keywords = {Genome Evolution},
pubstate = {published},
tppubtype = {article}
}
Large-scale rearrangements may be important in evolution because they can alter chromosome organization and gene expression in ways not possible through point mutations. In a long-term evolution experiment, twelve Escherichia coli populations have been propagated in a glucose-limited environment for over 25 years. We used whole-genome mapping (optical mapping) combined with genome sequencing and PCR analysis to identify the large-scale chromosomal rearrangements in clones from each population after 40,000 generations. A total of 110 rearrangement events were detected, including 82 deletions, 19 inversions, and 9 duplications, with lineages having between 5 and 20 events. In three populations, successive rearrangements impacted particular regions. In five populations, rearrangements affected over a third of the chromosome. Most rearrangements involved recombination between insertion sequence (IS) elements, illustrating their importance in mediating genome plasticity. Two lines of evidence suggest that at least some of these rearrangements conferred higher fitness. First, parallel changes were observed across the independent populations, with ~65% of the rearrangements affecting the same loci in at least two populations. For example, the ribose-utilization operon and the manB - cpsG region were deleted in 12 and 10 populations, respectively, suggesting positive selection, and this inference was previously confirmed for the former case. Second, optical maps from clones sampled over time from one population showed that most rearrangements occurred early in the experiment, when fitness was increasing most rapidly. However, some rearrangements likely occur at high frequency and may have simply hitchhiked to fixation. In any case, large-scale rearrangements clearly influenced genomic evolution in these populations.
Plucain J; Hindré T; Gac M L; Tenaillon O; Cruveiller S; Medigue C; Leiby N; Harcombe W R; Marx C J; Lenski R E; Schneider D
Epistasis and Allele Specificity in the Emergence of a Stable Polymorphism in Escherichia coli Journal Article
Science, 343 (6177), pp. 1366–1369, 2014, ISSN: 0036-8075.
Abstract | Links | BibTeX | Altmetric | Tags: Demography and Ecology, Genotypes and Phenotypes
@article{Plucain2014,
title = {Epistasis and Allele Specificity in the Emergence of a Stable Polymorphism in \textit{Escherichia coli}},
author = {Jessica Plucain and Thomas Hindré and Mickaël Le Gac and Olivier Tenaillon and Stéphane Cruveiller and Claudine Medigue and Nicholas Leiby and William R. Harcombe and Christopher J. Marx and Richard E. Lenski and Dominique Schneider},
url = {https://www.sciencemag.org/lookup/doi/10.1126/science.1248688},
doi = {10.1126/science.1248688},
issn = {0036-8075},
year = {2014},
date = {2014-03-01},
urldate = {2014-03-01},
journal = {Science},
volume = {343},
number = {6177},
pages = {1366--1369},
abstract = {Ecological opportunities promote population divergence into coexisting lineages. However, the genetic mechanisms that enable new lineages to exploit these opportunities are poorly understood except in cases of single mutations. We examined how two \textit{Escherichia coli} lineages diverged from their common ancestor at the outset of a long-term coexistence. By sequencing genomes and reconstructing the genetic history of one lineage, we showed that three mutations together were sufficient to produce the frequency-dependent fitness effects that allowed this lineage to invade and stably coexist with the other. These mutations all affected regulatory genes and collectively caused substantial metabolic changes. Moreover, the particular derived alleles were critical for the initial divergence and invasion, indicating that the establishment of this polymorphism depended on specific epistatic interactions.},
keywords = {Demography and Ecology, Genotypes and Phenotypes},
pubstate = {published},
tppubtype = {article}
}
Ecological opportunities promote population divergence into coexisting lineages. However, the genetic mechanisms that enable new lineages to exploit these opportunities are poorly understood except in cases of single mutations. We examined how two Escherichia coli lineages diverged from their common ancestor at the outset of a long-term coexistence. By sequencing genomes and reconstructing the genetic history of one lineage, we showed that three mutations together were sufficient to produce the frequency-dependent fitness effects that allowed this lineage to invade and stably coexist with the other. These mutations all affected regulatory genes and collectively caused substantial metabolic changes. Moreover, the particular derived alleles were critical for the initial divergence and invasion, indicating that the establishment of this polymorphism depended on specific epistatic interactions.
Quandt E M; Deatherage D E; Ellington A D; Georgiou G; Barrick J E
Recursive genomewide recombination and sequencing reveals a key refinement step in the evolution of a metabolic innovation in Escherichia coli Journal Article
Proceedings of the National Academy of Sciences, 111 (6), pp. 2217–2222, 2014, ISSN: 0027-8424.
Abstract | Links | BibTeX | Altmetric | Tags: Citrate Evolution, Genotypes and Phenotypes, Methods and Miscellaneous
@article{Quandt2014,
title = {Recursive genomewide recombination and sequencing reveals a key refinement step in the evolution of a metabolic innovation in \textit{Escherichia coli}},
author = {Erik M. Quandt and Daniel E. Deatherage and Andrew D. Ellington and George Georgiou and Jeffrey E. Barrick},
url = {http://www.pnas.org/lookup/doi/10.1073/pnas.1314561111},
doi = {10.1073/pnas.1314561111},
issn = {0027-8424},
year = {2014},
date = {2014-02-01},
urldate = {2014-02-01},
journal = {Proceedings of the National Academy of Sciences},
volume = {111},
number = {6},
pages = {2217--2222},
abstract = {Evolutionary innovations often arise from complex genetic and ecological interactions, which can make it challenging to understand retrospectively how a novel trait arose. In a long-term experiment, \textit{Escherichia coli} gained the ability to use abundant citrate (Cit+) in the growth medium after ~31,500 generations of evolution. Exploiting this previously untapped resource was highly beneficial: later Cit+ variants achieve a much higher population density in this environment. All Cit+ individuals share a mutation that activates aerobic expression of the \textit{citT} citrate transporter, but this mutation confers only an extremely weak Cit+ phenotype on its own. To determine which of the other >70 mutations in early Cit+ clones were needed to take full advantage of citrate, we developed a recursive genomewide recombination and sequencing method (REGRES) and performed genetic backcrosses to purge mutations not required for Cit+ from an evolved strain. We discovered a mutation that increased expression of the \textit{dctA} C4-dicarboxylate transporter greatly enhanced the Cit+ phenotype after it evolved. Surprisingly, strains containing just the \textit{citT} and \textit{dctA} mutations fully use citrate, indicating that earlier mutations thought to have potentiated the initial evolution of Cit+ are not required for expression of the refined version of this trait. Instead, this metabolic innovation may be contingent on a genetic background, and possibly ecological context, that enabled \textit{citT} mutants to persist among competitors long enough to obtain \textit{dctA} or equivalent mutations that conferred an overwhelming advantage. More generally, refinement of an emergent trait from a rudimentary form may be crucial to its evolutionary success.},
keywords = {Citrate Evolution, Genotypes and Phenotypes, Methods and Miscellaneous},
pubstate = {published},
tppubtype = {article}
}
Evolutionary innovations often arise from complex genetic and ecological interactions, which can make it challenging to understand retrospectively how a novel trait arose. In a long-term experiment, Escherichia coli gained the ability to use abundant citrate (Cit+) in the growth medium after ~31,500 generations of evolution. Exploiting this previously untapped resource was highly beneficial: later Cit+ variants achieve a much higher population density in this environment. All Cit+ individuals share a mutation that activates aerobic expression of the citT citrate transporter, but this mutation confers only an extremely weak Cit+ phenotype on its own. To determine which of the other >70 mutations in early Cit+ clones were needed to take full advantage of citrate, we developed a recursive genomewide recombination and sequencing method (REGRES) and performed genetic backcrosses to purge mutations not required for Cit+ from an evolved strain. We discovered a mutation that increased expression of the dctA C4-dicarboxylate transporter greatly enhanced the Cit+ phenotype after it evolved. Surprisingly, strains containing just the citT and dctA mutations fully use citrate, indicating that earlier mutations thought to have potentiated the initial evolution of Cit+ are not required for expression of the refined version of this trait. Instead, this metabolic innovation may be contingent on a genetic background, and possibly ecological context, that enabled citT mutants to persist among competitors long enough to obtain dctA or equivalent mutations that conferred an overwhelming advantage. More generally, refinement of an emergent trait from a rudimentary form may be crucial to its evolutionary success.
Leiby N; Marx C J
PLoS Biology, 12 (2), pp. e1001789, 2014, ISSN: 1545-7885.
Abstract | Links | BibTeX | Altmetric | Tags: Correlated Responses, Mutation Rates
@article{Leiby2014,
title = {Metabolic Erosion Primarily Through Mutation Accumulation, and Not Tradeoffs, Drives Limited Evolution of Substrate Specificity in \textit{Escherichia coli}},
author = {Nicholas Leiby and Christopher J. Marx},
editor = {Nancy A. Moran},
url = {https://dx.plos.org/10.1371/journal.pbio.1001789},
doi = {10.1371/journal.pbio.1001789},
issn = {1545-7885},
year = {2014},
date = {2014-02-01},
urldate = {2014-02-01},
journal = {PLoS Biology},
volume = {12},
number = {2},
pages = {e1001789},
abstract = {Evolutionary adaptation to a constant environment is often accompanied by specialization and a reduction of fitness in other environments. We assayed the ability of the Lenski \textit{Escherichia coli} populations to grow on a range of carbon sources after 50,000 generations of adaptation on glucose. Using direct measurements of growth rates, we demonstrated that declines in performance were much less widespread than suggested by previous results from Biolog assays of cellular respiration. Surprisingly, there were many performance increases on a variety of substrates. In addition to the now famous example of citrate, we observed several other novel gains of function for organic acids that the ancestral strain only marginally utilized. Quantitative growth data also showed that strains with a higher mutation rate exhibited significantly more declines, suggesting that most metabolic erosion was driven by mutation accumulation and not by physiological tradeoffs. These reductions in growth by mutator strains were ameliorated by growth at lower temperature, consistent with the hypothesis that this metabolic erosion is largely caused by destabilizing mutations to the associated enzymes. We further hypothesized that reductions in growth rate would be greatest for substrates used most differently from glucose, and we used flux balance analysis to formulate this question quantitatively. To our surprise, we found no significant relationship between decreases in growth and dissimilarity to glucose metabolism. Taken as a whole, these data suggest that in a single resource environment, specialization does not mainly result as an inevitable consequence of adaptive tradeoffs, but rather due to the gradual accumulation of disabling mutations in unused portions of the genome. },
keywords = {Correlated Responses, Mutation Rates},
pubstate = {published},
tppubtype = {article}
}
Evolutionary adaptation to a constant environment is often accompanied by specialization and a reduction of fitness in other environments. We assayed the ability of the Lenski Escherichia coli populations to grow on a range of carbon sources after 50,000 generations of adaptation on glucose. Using direct measurements of growth rates, we demonstrated that declines in performance were much less widespread than suggested by previous results from Biolog assays of cellular respiration. Surprisingly, there were many performance increases on a variety of substrates. In addition to the now famous example of citrate, we observed several other novel gains of function for organic acids that the ancestral strain only marginally utilized. Quantitative growth data also showed that strains with a higher mutation rate exhibited significantly more declines, suggesting that most metabolic erosion was driven by mutation accumulation and not by physiological tradeoffs. These reductions in growth by mutator strains were ameliorated by growth at lower temperature, consistent with the hypothesis that this metabolic erosion is largely caused by destabilizing mutations to the associated enzymes. We further hypothesized that reductions in growth rate would be greatest for substrates used most differently from glucose, and we used flux balance analysis to formulate this question quantitatively. To our surprise, we found no significant relationship between decreases in growth and dissimilarity to glucose metabolism. Taken as a whole, these data suggest that in a single resource environment, specialization does not mainly result as an inevitable consequence of adaptive tradeoffs, but rather due to the gradual accumulation of disabling mutations in unused portions of the genome.