Bacterial transcriptome reorganization in thermal adaptive evolution

Bei-Wen Ying, Yuki Matsumoto, Kazuki Kitahara, Shingo Suzuki, Naoaki Ono, Chikara Furusawa, Toshihiko Kishimoto, Tetsuya Yomo

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. 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. Evolved 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. Our 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.