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Global coordination in adaptation to gene rewiring.

Yoshie Murakami1, Yuki Matsumoto2, Saburo Tsuru1

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Gene rewiring can lead to extinction, but cells can adapt through stochastic gene expression. Successful adaptation involves cooperative operon and genome-wide gene expression changes, revealing a general path toward cellular plasticity.

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Area of Science:

  • Synthetic Biology
  • Evolutionary Biology
  • Genomics

Background:

  • Gene rewiring is a natural evolutionary process that can cause extinction.
  • Synthetic biology shows cells can survive genetic rewiring, often via stochastic gene expression.
  • The probability and principles of adaptation to gene rewiring remain unclear.

Purpose of the Study:

  • To systematically investigate the adaptation mechanisms of gene-rewired Escherichia coli strains.
  • To identify the common principles governing cellular survival and adaptation following genetic rewiring.
  • To understand the relationship between gene expression dynamics and cell fate.

Main Methods:

  • Systematic survey of diverse gene-rewired Escherichia coli strains.
  • Observation of cell fates (good survivors, poor survivors, failures) under starvation conditions.
  • Analysis of gene expression fluctuations, cell size, operon organization, and genome-wide transcriptomic changes.

Main Results:

  • Three distinct cell fates were observed in response to gene rewiring and starvation.
  • While fluctuations in rewired gene expression and increased cell size were common, they were insufficient for adaptation.
  • Cooperative operon and genome-wide gene expression reorganizations were crucial for successful adaptation.
  • Transcriptome dynamics, despite high dimensionality, followed a constrained one-dimensional trajectory toward adaptation.

Conclusions:

  • Successful adaptation to gene rewiring is not solely dependent on individual gene expression stochasticity but requires coordinated genomic and transcriptomic reorganization.
  • A general adaptive path, characterized by cellular plasticity, exists for gene-rewired cells.
  • Findings offer insights into designing complex genetic and metabolic networks and understanding evolutionary adaptation.