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The phenotypic signature of adaptation to thermal stress in Escherichia coli.

Hug SM, Gaut BS - BMC Evol. Biol. (2015)

Bottom Line: Phenotypic variation associated statistically with genetic variation, demonstrating a genetic basis for phenotypic change.Our results contribute to previous observations showing that a major component of adaptation in microbial evolution experiments is toward restoration to the unstressed state.In addition, we found that a large deletion strongly affected phenotypic variation.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, UC Irvine, 321 Steinhaus Hall, Irvine, CA, 92697, USA. shug@uci.edu.

ABSTRACT

Background: In the short-term, organisms acclimate to stress through phenotypic plasticity, but in the longer term they adapt to stress genetically. The mutations that accrue during adaptation may contribute to completely novel phenotypes, or they may instead act to restore the phenotype from a stressed to a pre-stress condition. To better understand the influence of evolution on the diversity and direction of phenotypic change, we used Biolog microarrays to assay 94 phenotypes of 115 Escherichia coli clones that had adapted to high temperature (42.2 °C). We also assayed these same phenotypes in the clones' ancestor under non-stress (37.0 °C) and stress (42.2 °C) conditions. We explored associations between Biolog phenotypes and genotypes, and we also investigated phenotypic differences between clones that have one of two adaptive genetic trajectories: one that is typified by mutations in the RNA polymerase β-subunit (rpoB) and another that is defined by mutations in the rho termination factor.

Results: Most (54 %) phenotypic variation was restorative, shifting the phenotype from the acclimated state back toward the unstressed state. Novel phenotypes were more rare, comprising between 5 and 18 % of informative phenotypic variation. Phenotypic variation associated statistically with genetic variation, demonstrating a genetic basis for phenotypic change. Finally, clones with rpoB mutations differed in phenotype from those with rho mutations, largely due to differences in chemical sensitivity.

Conclusions: Our results contribute to previous observations showing that a major component of adaptation in microbial evolution experiments is toward restoration to the unstressed state. In addition, we found that a large deletion strongly affected phenotypic variation. Finally, we demonstrated that the two genetic trajectories leading to thermal adaptation encompass different phenotypes.

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Plot of the first two principal components. The dots represent scores from the 115 evolved clones, each of which was replicated three times. The triangles represent the six replicates of the REL1206 ancestral strain at 42.2 °C; squares denote the ancestor at 37.0 °C. The arrows at the top of the plot illustrate directions of change relative to the two ancestral treatments (see Fig. 1 and Table 1)
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Fig2: Plot of the first two principal components. The dots represent scores from the 115 evolved clones, each of which was replicated three times. The triangles represent the six replicates of the REL1206 ancestral strain at 42.2 °C; squares denote the ancestor at 37.0 °C. The arrows at the top of the plot illustrate directions of change relative to the two ancestral treatments (see Fig. 1 and Table 1)

Mentions: Figure 2 plots the first and second principal components and helps convey two pieces of information about PCA scores. First, the ancestral data were typically well differentiated by treatment (37.0 or 42.2 °C). For example, the first component visually separated the sets of six ancestral replicates by treatment (Fig. 2). While the separation was less obvious for the second component, t-test comparisons between and indicated that the two ancestral treatments were significantly differentiated in seven of nine principal components (pc1, pc2, pc5, pc6, pc7, pc8 and pc9; t-test, unequal variances; sequential Bonferroni correction for α = 0.01). This differentiation represents the phenotypic effects of acclimation (Fig. 1).Fig. 2


The phenotypic signature of adaptation to thermal stress in Escherichia coli.

Hug SM, Gaut BS - BMC Evol. Biol. (2015)

Plot of the first two principal components. The dots represent scores from the 115 evolved clones, each of which was replicated three times. The triangles represent the six replicates of the REL1206 ancestral strain at 42.2 °C; squares denote the ancestor at 37.0 °C. The arrows at the top of the plot illustrate directions of change relative to the two ancestral treatments (see Fig. 1 and Table 1)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4557228&req=5

Fig2: Plot of the first two principal components. The dots represent scores from the 115 evolved clones, each of which was replicated three times. The triangles represent the six replicates of the REL1206 ancestral strain at 42.2 °C; squares denote the ancestor at 37.0 °C. The arrows at the top of the plot illustrate directions of change relative to the two ancestral treatments (see Fig. 1 and Table 1)
Mentions: Figure 2 plots the first and second principal components and helps convey two pieces of information about PCA scores. First, the ancestral data were typically well differentiated by treatment (37.0 or 42.2 °C). For example, the first component visually separated the sets of six ancestral replicates by treatment (Fig. 2). While the separation was less obvious for the second component, t-test comparisons between and indicated that the two ancestral treatments were significantly differentiated in seven of nine principal components (pc1, pc2, pc5, pc6, pc7, pc8 and pc9; t-test, unequal variances; sequential Bonferroni correction for α = 0.01). This differentiation represents the phenotypic effects of acclimation (Fig. 1).Fig. 2

Bottom Line: Phenotypic variation associated statistically with genetic variation, demonstrating a genetic basis for phenotypic change.Our results contribute to previous observations showing that a major component of adaptation in microbial evolution experiments is toward restoration to the unstressed state.In addition, we found that a large deletion strongly affected phenotypic variation.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolutionary Biology, UC Irvine, 321 Steinhaus Hall, Irvine, CA, 92697, USA. shug@uci.edu.

ABSTRACT

Background: In the short-term, organisms acclimate to stress through phenotypic plasticity, but in the longer term they adapt to stress genetically. The mutations that accrue during adaptation may contribute to completely novel phenotypes, or they may instead act to restore the phenotype from a stressed to a pre-stress condition. To better understand the influence of evolution on the diversity and direction of phenotypic change, we used Biolog microarrays to assay 94 phenotypes of 115 Escherichia coli clones that had adapted to high temperature (42.2 °C). We also assayed these same phenotypes in the clones' ancestor under non-stress (37.0 °C) and stress (42.2 °C) conditions. We explored associations between Biolog phenotypes and genotypes, and we also investigated phenotypic differences between clones that have one of two adaptive genetic trajectories: one that is typified by mutations in the RNA polymerase β-subunit (rpoB) and another that is defined by mutations in the rho termination factor.

Results: Most (54 %) phenotypic variation was restorative, shifting the phenotype from the acclimated state back toward the unstressed state. Novel phenotypes were more rare, comprising between 5 and 18 % of informative phenotypic variation. Phenotypic variation associated statistically with genetic variation, demonstrating a genetic basis for phenotypic change. Finally, clones with rpoB mutations differed in phenotype from those with rho mutations, largely due to differences in chemical sensitivity.

Conclusions: Our results contribute to previous observations showing that a major component of adaptation in microbial evolution experiments is toward restoration to the unstressed state. In addition, we found that a large deletion strongly affected phenotypic variation. Finally, we demonstrated that the two genetic trajectories leading to thermal adaptation encompass different phenotypes.

Show MeSH
Related in: MedlinePlus