Abstract
BackgroundEvolution optimizes a living system at both the genome and transcriptome levels. Few studies have investigated transcriptome evolution, whereas many studies have explored genome evolution in experimentally evolved cells. However, a comprehensive understanding of evolutionary mechanisms requires knowledge of how evolution shapes gene expression. Here, we analyzed Escherichia coli strains acquired during long-term thermal adaptive evolution.ResultsEvolved and ancestor Escherichia coli cells were exponentially grown under normal and high temperatures for subsequent transcriptome analysis. We found that both the ancestor and evolved cells had comparable magnitudes of transcriptional change in response to heat shock, although the evolutionary progression of their expression patterns during exponential growth was different at either normal or high temperatures. We also identified inverse transcriptional changes that were mediated by differences in growth temperatures and genotypes, as well as negative epistasis between genotype—and heat shock-induced transcriptional changes. Principal component analysis revealed that transcriptome evolution neither approached the responsive state at the high temperature nor returned to the steady state at the regular temperature. We propose that the molecular mechanisms of thermal adaptive evolution involve the optimization of steady-state transcriptomes at high temperatures without disturbing the heat shock response.ConclusionsOur results suggest that transcriptome evolution works to maintain steady-state gene expression during constrained differentiation at various evolutionary stages, while also maintaining responsiveness to environmental stimuli and transcriptome homeostasis.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1999-x) contains supplementary material, which is available to authorized users.
Highlights
Evolution optimizes a living system at both the genome and transcriptome levels
Overview of transcriptome evolution for thermal adaptation To identify changes in gene expression for thermal adaptation, four Escherichia coli strains were acquired during experimental evolution that we performed previously [5]
The results showed that the evolved cells demonstrated highly recovered growth fitness at their corresponding evolutionary temperatures (Fig. 1b), consistent with our previous report [5]. These growing cells were collected for microarray analysis, such that growth rates corresponded to transcriptomes at the exponential growing phases analyzed in this study (Additional file 1: Figure S1)
Summary
Evolution optimizes a living system at both the genome and transcriptome levels. Few studies have investigated transcriptome evolution, whereas many studies have explored genome evolution in experimentally evolved cells. Evolutionary experimentation is a powerful tool for the exploration of how living organisms adapt to environmental change and is commonly applied in studies of evolution, typically focusing on changes in genome sequences. The results of these studies have provided experimental evidence to substantiate or revise numerous theories of evolution [1, 2]; the evolutionary mechanisms were generally explained by changes in DNA sequences and/or some particular genes [3,4,5,6]. Adaptive evolution works to optimize cellular gene expression; transcriptome evolution is a relevant area of study. Our previous studies identified transcriptome-wide growth-induced transcriptome reorganization [18] and demonstrated that a similar global coordination was found for
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