Collective peroxide detoxification determines microbial mutation rate plasticity in E. coli

PLoS Biol. 2024 Jul 15;22(7):e3002711. doi: 10.1371/journal.pbio.3002711. eCollection 2024 Jul.

Abstract

Mutagenesis is responsive to many environmental factors. Evolution therefore depends on the environment not only for selection but also in determining the variation available in a population. One such environmental dependency is the inverse relationship between mutation rates and population density in many microbial species. Here, we determine the mechanism responsible for this mutation rate plasticity. Using dynamical computational modelling and in culture mutation rate estimation, we show that the negative relationship between mutation rate and population density arises from the collective ability of microbial populations to control concentrations of hydrogen peroxide. We demonstrate a loss of this density-associated mutation rate plasticity (DAMP) when Escherichia coli populations are deficient in the degradation of hydrogen peroxide. We further show that the reduction in mutation rate in denser populations is restored in peroxide degradation-deficient cells by the presence of wild-type cells in a mixed population. Together, these model-guided experiments provide a mechanistic explanation for DAMP, applicable across all domains of life, and frames mutation rate as a dynamic trait shaped by microbial community composition.

MeSH terms

  • Escherichia coli* / drug effects
  • Escherichia coli* / genetics
  • Escherichia coli* / metabolism
  • Hydrogen Peroxide / metabolism
  • Hydrogen Peroxide / pharmacology
  • Inactivation, Metabolic / genetics
  • Mutation
  • Mutation Rate*

Substances

  • Hydrogen Peroxide

Grants and funding

RG is supported by Biotechnology and Biological Sciences Research Council (BBSRC) DTP BB/T008725/1 https://www.ukri.org/councils/bbsrc/. RK is supported by the UK Research and Innovation (UKRI) Future Leaders Fellowship MR/T021225/1 https://www.ukri.org/. PP is supported by Biotechnology and Biological Sciences Research Council (BBSRC) research grant BB/R007691/1 https://www.ukri.org/councils/bbsrc/. All sponsors played no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.