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. 2017 Mar 7;114(10):E1904-E1912.
doi: 10.1073/pnas.1616132114. Epub 2017 Feb 15.

Specificity of Genome Evolution in Experimental Populations of Escherichia coli Evolved at Different Temperatures

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Free PMC article

Specificity of Genome Evolution in Experimental Populations of Escherichia coli Evolved at Different Temperatures

Daniel E Deatherage et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

Isolated populations derived from a common ancestor are expected to diverge genetically and phenotypically as they adapt to different local environments. To examine this process, 30 populations of Escherichia coli were evolved for 2,000 generations, with six in each of five different thermal regimes: constant 20 °C, 32 °C, 37 °C, 42 °C, and daily alternations between 32 °C and 42 °C. Here, we sequenced the genomes of one endpoint clone from each population to test whether the history of adaptation in different thermal regimes was evident at the genomic level. The evolved strains had accumulated ∼5.3 mutations, on average, and exhibited distinct signatures of adaptation to the different environments. On average, two strains that evolved under the same regime exhibited ∼17% overlap in which genes were mutated, whereas pairs that evolved under different conditions shared only ∼4%. For example, all six strains evolved at 32 °C had mutations in nadR, whereas none of the other 24 strains did. However, a population evolved at 37 °C for an additional 18,000 generations eventually accumulated mutations in the signature genes strongly associated with adaptation to the other temperature regimes. Two mutations that arose in one temperature treatment tended to be beneficial when tested in the others, although less so than in the regime in which they evolved. These findings demonstrate that genomic signatures of adaptation can be highly specific, even with respect to subtle environmental differences, but that this imprint may become obscured over longer timescales as populations continue to change and adapt to the shared features of their environments.

Keywords: experimental evolution; genome evolution; mutation; natural selection; temperature.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Genomic changes in E. coli evolved under different temperature regimes. (A) Overview of the TEE. E. coli clone REL1206 was isolated from the LTEE after 2,000 generations of evolution at 37 °C. In the TEE, six populations evolved for 2,000 generations in each of five different temperature treatments. Three populations in each treatment started from Ara clone REL1206 (designated −1, −2, −3) and three from Ara+ clone REL1207 (+1, +2, +3), which differs from REL1206 by a single point mutation that is neutral with respect to fitness. (B) Summary of the 159 derived mutations observed in the 30 sequenced TEE genomes by the type of genetic change.
Fig. 2.
Fig. 2.
Mutations in several signature genes are associated with evolution under different temperature regimes. (A) Temperature treatments and edges connecting them are labeled with Dice similarity scores that represent the average percentage of mutated genes in common among all genome pairs within each treatment (Sw) and the average across all genome pairs between two treatments (Sb), respectively. Only the 132 qualifying mutations that affect a single gene were included in these calculations. The difference between Sb and Sw, indicating a temperature-specific pattern of genomic evolution, is significant (P < 0.05, randomization test with sequential Bonferroni correction) for all treatment pairs except the combination of the Switch (alternating 32 °C and 42 °C) and 42 °C regimes (dashed line). (B) Genes (rows) affected by at least two qualifying mutations in the 30 TEE clones (columns, organized by temperature regime and populations –1, +1, –2, +2, –3, or +3). The five signature mutations, shown as colored squares, are significantly associated with one or two treatments (see Gene Targets That Contribute to Evolved Thermal Specificity). All other mutations are depicted as black circles.
Fig. 3.
Fig. 3.
Genes that are targets of selection in the TEE often accumulated mutations later in the LTEE at 37 °C. For each TEE treatment, we calculated an RI equal to the percentage of mutations affecting single genes in those six genomes that also experienced mutations in clones from the same LTEE population that produced the TEE progenitor. We calculated RI values for comparisons to LTEE clones sampled at 5K, 10K, and 20K. The TEE began from a 2000-generation clone from this population, so these LTEE clones had evolved for 3,000, 8,000, and 18,000 additional generations at constant 37 °C. As expected, the 37 °C treatment had a significantly higher RI at 5K and 10K than the other four treatments combined (P < 0.05, one-tailed Fisher’s Exact Test). This difference was no longer significant at 20K. This convergence supports the hypothesis that many of the mutations that arose in the different temperature treatments, which all shared the same nutrient and other conditions with the LTEE, also improve fitness at 37 °C, although to a lesser degree, thus accounting for their later emergence at that ancestral temperature.
Fig. 4.
Fig. 4.
Temperature specificity of beneficial mutations from two TEE populations. Two mutations that evolved during the TEE were moved into the ancestral genetic background. The resulting constructed strains then competed against a neutrally marked variant of the ancestor in each of five thermal regimes. Temperatures used for these competitions differed slightly from those used in the TEE (Materials and Methods). Error bars show 95% confidence intervals estimated from a one-way ANOVA. For treatments marked with one or two asterisks, the relative fitness of the strain with the evolved mutation was greater than one at P < 0.05 or P < 0.01, respectively (one-tailed t tests). (A) Results for the nadR mutation from the clone designated 32+3 (REL2042), which is a 2-bp deletion that causes a frameshift in the protein-coding sequence at amino acid 105. (B) Results for the aceB mutation from clone Sw−1 (REL2052), which is an A→C base change that causes a glutamate to alanine substitution at amino acid 69. This aceB mutation is expected to have an effect on cellular metabolism similar to that of the iclR mutations that were common in the 42 °C and Switch treatments (see Gene Targets That Contribute to Evolved Thermal Specificity).

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