Long-Term Experimental Evolution in Escherichia coli. IX. Characterization of Insertion Sequence-Mediated Mutations and Rearrangements

Genetics ◽  
2000 ◽  
Vol 156 (2) ◽  
pp. 477-488
Author(s):  
Dominique Schneider ◽  
Esther Duperchy ◽  
Evelyne Coursange ◽  
Richard E Lenski ◽  
Michel Blot
Keyword(s):  
Escherichia Coli ◽  
Experimental Evolution ◽  
Insertion Sequence ◽  
Term Evolution ◽  
Molecular Events ◽  
Evolution Experiment ◽  
Two Populations ◽  
Escherichia Coli B

Abstract As part of a long-term evolution experiment, two populations of Escherichia coli B adapted to a glucose minimal medium for 10,000 generations. In both populations, multiple IS-associated mutations arose that then went to fixation. We identify the affected genetic loci and characterize the molecular events that produced nine of these mutations. All nine were IS-mediated events, including simple insertions as well as recombination between homologous elements that generated inversions and deletions. Sequencing DNA adjacent to the insertions indicates that the affected genes are involved in central metabolism (knockouts of pykF and nadR), cell wall synthesis (adjacent to the promoter of pbpA-rodA), and ill-defined functions (knockouts of hokB-sokB and yfcU). These genes are candidates for manipulation and competition experiments to determine whether the mutations were beneficial or merely hitchhiked to fixation.

scholarly journals Selection maintains protein interactome resilience in the long-term evolution experiment with Escherichia coli

2021 ◽  
Author(s):  
Rohan Maddamsetti
Keyword(s):  
Experimental Evolution ◽  
Long Term Evolution ◽  
Rate Of Change ◽  
Network Resilience ◽  
Protein Protein Interaction ◽  
Ppi Networks ◽  
Term Evolution ◽  
Protein Interactome ◽  
Evolution Experiment

AbstractMost cellular functions are carried out by a dynamic network of interacting proteins. An open question is whether the network properties of protein interactomes represent phenotypes under natural selection. One proposal is that protein interactomes have evolved to be resilient, such that they tend to maintain connectivity when proteins are removed from the network. This hypothesis predicts that interactome resilience should be maintained during long-term experimental evolution. I tested this prediction by modeling the evolution of protein-protein interaction (PPI) networks in Lenski’s long-term evolution experiment with Escherichia coli (LTEE). In this test, I removed proteins affected by nonsense, insertion, deletion, and transposon mutations in evolved LTEE strains, and measured the resilience of the resulting networks. I compared the rate of change of network resilience in each LTEE population to the rate of change of network resilience for corresponding randomized networks. The evolved PPI networks are significantly more resilient than networks in which random proteins have been deleted. Moreover, the evolved networks are generally more resilient than networks in which the random deletion of proteins was restricted to those disrupted in LTEE. These results suggest that evolution in the LTEE has favored PPI networks that are, on average, more resilient than expected from the genetic variation across the evolved populations. My findings therefore support the hypothesis that selection maintains protein interactome resilience over evolutionary time.Significance StatementUnderstanding how protein-protein interaction (PPI) networks evolve is a central goal of evolutionary systems biology. One property that has been hypothesized to be important for PPI network evolution is resilience, which means that networks tend to maintain connectivity even after many nodes (proteins in this case) have been removed. This hypothesis predicts that PPI network resilience should be maintained during long-term experimental evolution. Consistent with this prediction, I found that the PPI networks that evolved over 50,000 generations of Lenski’s long-term evolution experiment with E. coli are more resilient than expected by chance.

scholarly journals Mutation Rate Inferred From Synonymous Substitutions in a Long-Term Evolution Experiment With Escherichia coli

2011 ◽  
Vol 1 (3) ◽  
pp. 183-186 ◽  
Author(s):  
Sébastien Wielgoss ◽  
Jeffrey E. Barrick ◽  
Olivier Tenaillon ◽  
Stéphane Cruveiller ◽  
Béatrice Chane-Woon-Ming ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Mutation Rate ◽  
Long Term Evolution ◽  
Synonymous Substitutions ◽  
Term Evolution ◽  
Evolution Experiment

scholarly journals Universal constraints on protein evolution in the long-term evolution experiment with Escherichia coli

2021 ◽  
Author(s):  
Rohan Maddamsetti
Keyword(s):  
Escherichia Coli ◽  
Protein Evolution ◽  
Long Term Evolution ◽  
Protein Abundance ◽  
Nonsynonymous Mutation ◽  
Protein Protein Interaction ◽  
Term Evolution ◽  
Mutation Density ◽  
Evolution Experiment

Abstract Although it is well known that abundant proteins evolve slowly across the tree of life, there is little consensus for why this is true. Here, I report that abundant proteins evolve slowly in the hypermutator populations of Lenski’s long-term evolution experiment with Escherichia coli (LTEE). Specifically, the density of all observed mutations per gene, as measured in metagenomic time series covering 60,000 generations of the LTEE, significantly anti-correlates with mRNA abundance, protein abundance, and degree of protein-protein interaction. The same pattern holds for nonsynonymous mutation density. However, synonymous mutation density, measured across the LTEE hypermutator populations, positively correlates with protein abundance. These results show that universal constraints on protein evolution are visible in data spanning three decades of experimental evolution. Therefore, it should be possible to design experiments to answer why abundant proteins evolve slowly.

scholarly journals Divergent evolution of mutation rates and biases in the long-term evolution experiment with Escherichia coli

2020 ◽  
Author(s):  
Rohan Maddamsetti ◽  
Nkrumah A. Grant
Keyword(s):  
Escherichia Coli ◽  
Point Mutations ◽  
Long Term Evolution ◽  
Dna Topology ◽  
Mutation Rates ◽  
Rate Variation ◽  
Historical Contingency ◽  
Term Evolution ◽  
Evolution Experiment

ABSTRACTAll organisms encode enzymes that replicate, maintain, pack, recombine, and repair their genetic material. For this reason, mutation rates and biases also evolve by mutation, variation, and natural selection. By examining metagenomic time series of the Lenski long-term evolution experiment (LTEE) with Escherichia coli (Good, et al. 2017), we find that local mutation rate variation has evolved during the LTEE. Each LTEE population has evolved idiosyncratic differences in their rates of point mutations, indels, and mobile element insertions, due to the fixation of various hypermutator and antimutator alleles. One LTEE population, called Ara+3, shows a strong, symmetric wave pattern in its density of point mutations, radiating from the origin of replication. This pattern is largely missing from the other LTEE populations, most of which evolved missense, indel, or structural mutations in topA, fis, and dusB— loci that all affect DNA topology. The distribution of mutations in those genes over time suggests epistasis and historical contingency in the evolution of DNA topology, which may have in turn affected local mutation rates. Overall, the replicate populations of the LTEE have largely diverged in their mutation rates and biases, even though they have adapted to identical abiotic conditions.

scholarly journals Core Genes Evolve Rapidly in the Long-term Evolution Experiment with Escherichia coli

2016 ◽  
Author(s):  
Rohan Maddamsetti ◽  
Philip J. Hatcher ◽  
Anna G. Green ◽  
Barry L. Williams ◽  
Debora S. Marks ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Positive Selection ◽  
Long Term Evolution ◽  
Fine Tuning ◽  
Adaptive Mutations ◽  
E Coli ◽  
Term Evolution ◽  
Evolution Experiment ◽  
Core Genes

AbstractBacteria 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 are fast evolving in the long-term evolution experiment with Escherichia coli (LTEE) have also diversified extensively in nature. 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 fine-tune protein functions, rather than merely knocking them out. The LTEE conditions are novel for E. coli, at least in relation to the long sweep of its evolution in nature. The constancy and simplicity of the environment likely favor the complete loss of some unused functions and the fine-tuning of others.Competing Interests StatementWe, the authors, declare that we have no conflicts of interest.

scholarly journals Idiosyncratic purifying selection on metabolic enzymes in the long-term evolution experiment with Escherichia coli

2021 ◽  
Author(s):  
Rohan Maddamsetti
Keyword(s):  
Escherichia Coli ◽  
Purifying Selection ◽  
Metabolic Enzymes ◽  
Long Term Evolution ◽  
Central Metabolism ◽  
Loss Of Function ◽  
Deep Time ◽  
Term Evolution ◽  
Evolution Experiment

AbstractBacteria, Archaea, and Eukarya all share a common set of metabolic reactions. This implies that the function and topology of central metabolism has been evolving under purifying selection over deep time. Central metabolism may similarly evolve under purifying selection during longterm evolution experiments, although it is unclear how long such experiments would have to run (decades, centuries, millennia) before signs of purifying selection on metabolism appear. I hypothesized that central and superessential metabolic enzymes would show evidence of purifying selection in the long-term evolution experiment with Escherichia coli (LTEE), in which 12 initially identical bacterial populations have been evolving in the laboratory for more than 30 years and 60,000 bacterial generations. I also hypothesized that enzymes that specialize on single substrates would show stronger evidence of purifying selection in the LTEE than generalist enzymes that catalyze multiple reactions. I tested these hypotheses by analyzing metagenomic time series covering 60,000 generations of the LTEE. I find mixed support for these hypotheses: patterns of purifying selection on metabolic enzymes, at least after 60,000 generations of experimental evolution, are largely idiosyncratic and population-specific.Significance StatementPurifying selection conserves organismal function over evolutionary time. I looked for evidence of purifying selection on metabolic enzymes in an ongoing long-term evolution experiment with E. coli. While some populations show signs of purifying selection, the overall pattern is inconsistent. To explain this finding, I propose that each population’s metabolism is evolving in a molecular game of Jenga. In this conceptual model, loss-of-function mutations degrade costly, redundant, and inessential metabolic functions, after which purifying selection begins to dominate. The threshold at which purifying selection activates depends on the idiosyncratic trajectory of lost redundancies in each population.

scholarly journals Core Genes Evolve Rapidly in the Long-Term Evolution Experiment with Escherichia coli

2017 ◽  
Vol 9 (4) ◽  
pp. 1072-1083 ◽  
Author(s):  
Rohan Maddamsetti ◽  
Philip J. Hatcher ◽  
Anna G. Green ◽  
Barry L. Williams ◽  
Debora S. Marks ◽  
...  
Keyword(s):  
Escherichia Coli ◽  
Long Term Evolution ◽  
Term Evolution ◽  
Evolution Experiment ◽  
Core Genes

scholarly journals Divergent Evolution of Mutation Rates and Biases in the Long-Term Evolution Experiment with Escherichia coli

2020 ◽  
Vol 12 (9) ◽  
pp. 1591-1603 ◽  
Author(s):  
Rohan Maddamsetti ◽  
Nkrumah A Grant
Keyword(s):  
Escherichia Coli ◽  
Point Mutations ◽  
Long Term Evolution ◽  
Dna Topology ◽  
Mutation Rates ◽  
Rate Variation ◽  
Historical Contingency ◽  
Term Evolution ◽  
Evolution Experiment

Abstract All organisms encode enzymes that replicate, maintain, pack, recombine, and repair their genetic material. For this reason, mutation rates and biases also evolve by mutation, variation, and natural selection. By examining metagenomic time series of the Lenski long-term evolution experiment (LTEE) with Escherichia coli (Good BH, McDonald MJ, Barrick JE, Lenski RE, Desai MM. 2017. The dynamics of molecular evolution over 60,000 generations. Nature 551(7678):45–50.), we find that local mutation rate variation has evolved during the LTEE. Each LTEE population has evolved idiosyncratic differences in their rates of point mutations, indels, and mobile element insertions, due to the fixation of various hypermutator and antimutator alleles. One LTEE population, called Ara+3, shows a strong, symmetric wave pattern in its density of point mutations, radiating from the origin of replication. This pattern is largely missing from the other LTEE populations, most of which evolved missense, indel, or structural mutations in topA, fis, and dusB—loci that all affect DNA topology. The distribution of mutations in those genes over time suggests epistasis and historical contingency in the evolution of DNA topology, which may have in turn affected local mutation rates. Overall, the replicate populations of the LTEE have largely diverged in their mutation rates and biases, even though they have adapted to identical abiotic conditions.

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