Functional specialization in regulation and quality control in thermal adaptive evolution

Kazuma Yama, Yuki Matsumoto, Yoshie Murakami, Shigeto Seno, Hideo Matsuda, Kazuyoshi Goto, Daisuke Motooka, Shota Nakamura, Bei Wen Ying, Tetsuya Yomo

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Distinctive survival strategies, specialized in regulation and in quality control, were observed in thermal adaptive evolution with a laboratory Escherichia coli strain. The two specialists carried a single mutation either within rpoH or upstream of groESL, which led to the activated global regulation by sigma factor 32 or an increased amount of GroEL/ES chaperonins, respectively. Although both specialists succeeded in thermal adaptation, the common winner of the evolution was the specialist in quality control, that is, the strategy of chaperonin-mediated protein folding. To understand this evolutionary consequence, multilevel analyses of cellular status, for example, transcriptome, protein and growth fitness, were carried out. The specialist in quality control showed less change in transcriptional reorganization responding to temperature increase, which was consistent with the finding of that the two specialists showed the biased expression of molecular chaperones. Such repressed changes in gene expression seemed to be advantageous for long-term sustainability because a specific increase in chaperonins not only facilitated the folding of essential gene products but also saved cost in gene expression compared with the overall transcriptional increase induced by rpoH regulation. Functional specialization offered two strategies for successful thermal adaptation, whereas the evolutionary advantageous was more at the points of cost-saving in gene expression and the essentiality in protein folding.

Original languageEnglish
Pages (from-to)943-955
Number of pages13
JournalGenes to Cells
Volume20
Issue number11
DOIs
Publication statusPublished - Nov 1 2015
Externally publishedYes

Fingerprint

Quality Control
Hot Temperature
Chaperonins
Protein Folding
Gene Expression
Multilevel Analysis
Costs and Cost Analysis
Molecular Chaperones
Essential Genes
Transcriptome
Escherichia coli
Mutation
Temperature
Growth
Proteins
Thermotolerance

ASJC Scopus subject areas

  • Genetics
  • Cell Biology

Cite this

Yama, K., Matsumoto, Y., Murakami, Y., Seno, S., Matsuda, H., Goto, K., ... Yomo, T. (2015). Functional specialization in regulation and quality control in thermal adaptive evolution. Genes to Cells, 20(11), 943-955. https://doi.org/10.1111/gtc.12298

Functional specialization in regulation and quality control in thermal adaptive evolution. / Yama, Kazuma; Matsumoto, Yuki; Murakami, Yoshie; Seno, Shigeto; Matsuda, Hideo; Goto, Kazuyoshi; Motooka, Daisuke; Nakamura, Shota; Ying, Bei Wen; Yomo, Tetsuya.

In: Genes to Cells, Vol. 20, No. 11, 01.11.2015, p. 943-955.

Research output: Contribution to journalArticle

Yama, K, Matsumoto, Y, Murakami, Y, Seno, S, Matsuda, H, Goto, K, Motooka, D, Nakamura, S, Ying, BW & Yomo, T 2015, 'Functional specialization in regulation and quality control in thermal adaptive evolution', Genes to Cells, vol. 20, no. 11, pp. 943-955. https://doi.org/10.1111/gtc.12298
Yama, Kazuma ; Matsumoto, Yuki ; Murakami, Yoshie ; Seno, Shigeto ; Matsuda, Hideo ; Goto, Kazuyoshi ; Motooka, Daisuke ; Nakamura, Shota ; Ying, Bei Wen ; Yomo, Tetsuya. / Functional specialization in regulation and quality control in thermal adaptive evolution. In: Genes to Cells. 2015 ; Vol. 20, No. 11. pp. 943-955.
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