The phenotypic signature of adaptation to thermal stress in Escherichia coli

Abstract

BackgroundIn 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.ResultsMost (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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0457-3) contains supplementary material, which is available to authorized users.

Evolutionary contingency’s impact on laboratory evolution ofEscherichia coliunder fluctuating environments

“…This phenotypic evaluation allows us to study the consequences of the evolutionary adaptation to our conditions in other regions of the ecological niche. Additionally, the resulting phenotypic signature can also be used as a proxy to study the hypothesized restorative effects of the accumulated mutations during adaptive laboratory evolution experiments, which is conjectured to bring the phenotypic signature closer to that of the unstressed environment (Hug & Gaut 2015). Here, we extend this hypothesis to the evolutionary response in complex environmental treatments.…”

MALDI-TOF Mass Spectrometry Enables a Comprehensive and Fast Analysis of Dynamics and Qualities of Stress Responses of Lactobacillus paracasei subsp. paracasei F19

“…Van de Guchte et al . reviewed that short-term stress responses primarily lead to the activation or stabilization of small proteins which are already present [7], whereas long-term adaptation processes to environmental stress evoke changes in membrane compositions [71]. Furthermore, the ability to quickly respond to environmental stress is essential for LAB in order to survive [72].…”

Evolutionary Pathway Determines the Stoichiometric Response of Escherichia coli Adapted to High Temperature

“…There are two broad conceptual models for how adaptation might affect cellular biochemistry and stoichiometry: adaptations could restore the organism to it normal pre-stressed physiological state or acclimation phenotypes could be reinforced by adaptations (Hug and Gaut, 2015). Physiologically in E. coli, protein degradation as well as peptide elongation rates increase at high temperature, resulting in a higher turnover of peptides (Farewell and Neidhardt, 1998).…”

“…Nonetheless, there were some lines that did have mutations in both genes, although they did not include either of the most prevalent rho and rpoB mutations. Phenotypic differences between cells with rho and rpoB mutations were identified using Biolog plates (Hug and Gaut, 2015). The strongest differences between rho and rpoB lines were among chemical sensitivity, but also included differential amino acid usage, suggesting there may be differences in their resource requirements (Hug and Gaut, 2015).…”

“…Phenotypic differences between cells with rho and rpoB mutations were identified using Biolog plates (Hug and Gaut, 2015). The strongest differences between rho and rpoB lines were among chemical sensitivity, but also included differential amino acid usage, suggesting there may be differences in their resource requirements (Hug and Gaut, 2015). The gene rpoB encodes the β subunit of RNA polymerase and may increase the capacity of cell lines to adapt (Barrick et al, 2010).…”