Bacterial transcriptome reorganization in thermal adaptive evolution

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.

Correlation between genome reduction and bacterial growth

“…1B). In addition, the genes located in the deleted regions were clustered according to the gene categories (summarized in Supplementary Table S1) and subjected to enrichment analysis to identify the significant loss of gene function in each strain (reduced genomes), as previously reported 29 , 30 , 31 . Bimodal tests revealed that the deleted genomic sequences were most significantly enriched in the gene category of phage/IS-related function (h) (Supplementary Fig.…”

“…Such a global effect of bacterial growth has been demonstrated by the correlation between transcriptome and growth fitness 27 , 28 in both adaptation 29 , 30 and evolution 31 . However, studies constructing reduced genomes have reported diverse evidence regarding growth.…”

Coordinated Changes in Mutation and Growth Rates Induced by Genome Reduction

“…The biological replicates were averaged to generate a representative gene expression value under each condition. The growth data sets of the exponentially growing E. coli cells were adopted from the associated papers ( 30 , 40 – 42 ).…”

The Escherichia coli transcriptome linked to growth fitness

“…Our studies critically consider the correlation between cell growth rate and the transcriptome. Thus, the following experimental procedures, which were excluded from the Materials and Methods of the original papers [4] , [5] , [6] , were performed. The details described here can be used to reproduce our deposited transcriptome data sets and the corresponding analytical results.…”

“…The genetic backgrounds of the Escherichia coli ( E. coli ) strains used for the transcriptome analyses are in previous reports [4] , [5] , [6] . An overview of these strains is shown in the Specifications table in the Data in Brief .…”