Spurious regulatory connections dictate the expression-fitness landscape of translation factors

Mol Syst Biol. 2021 Apr;17(4):e10302. doi: 10.15252/msb.202110302.

Abstract

During steady-state cell growth, individual enzymatic fluxes can be directly inferred from growth rate by mass conservation, but the inverse problem remains unsolved. Perturbing the flux and expression of a single enzyme could have pleiotropic effects that may or may not dominate the impact on cell fitness. Here, we quantitatively dissect the molecular and global responses to varied expression of translation termination factors (peptide release factors, RFs) in the bacterium Bacillus subtilis. While endogenous RF expression maximizes proliferation, deviations in expression lead to unexpected distal regulatory responses that dictate fitness reduction. Molecularly, RF depletion causes expression imbalance at specific operons, which activates master regulators and detrimentally overrides the transcriptome. Through these spurious connections, RF abundances are thus entrenched by focal points within the regulatory network, in one case located at a single stop codon. Such regulatory entrenchment suggests that predictive bottom-up models of expression-fitness landscapes will require near-exhaustive characterization of parts.

Keywords: expression-fitness landscape; multiscale measurements; peptide chain release factors; regulatory entrenchment; translation factors.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Bacillus subtilis / genetics*
  • Bacterial Proteins / metabolism
  • Base Sequence
  • CRISPR-Cas Systems / genetics
  • Gene Expression Regulation, Bacterial*
  • Genome, Bacterial
  • Peptide Termination Factors / metabolism*
  • Protein Biosynthesis*
  • Proteome / metabolism
  • Stress, Physiological / genetics
  • Transcription, Genetic

Substances

  • Bacterial Proteins
  • Peptide Termination Factors
  • Proteome

Associated data

  • GEO/GSE162169