Chloramphenicol and gentamicin reduce the evolution of resistance to phage ΦX174 by suppressing a subset of E. coli LPS mutants

PLoS Biol. 2025 Jan 21;23(1):e3002952. doi: 10.1371/journal.pbio.3002952. eCollection 2025 Jan.

Abstract

Bacteriophages infect gram-negative bacteria by attaching to molecules present on the bacterial surface, often lipopolysaccharides (LPS). Modification of LPS can lead to resistance to phage infection. In addition, LPS modifications can impact antibiotic susceptibility, allowing for phage-antibiotic synergism. The evolutionary mechanism(s) behind such synergistic interactions remain largely unclear. Here, we show that the presence of antibiotics can affect the evolution of resistance to phage infection, using phage ΦX174 and Escherichia coli C. We use a collection of 34 E. coli C LPS strains, each of which is resistant to ΦX174, and has either a "rough" or "deep rough" LPS phenotype. Growth of the bacterial strains with the deep rough phenotype is inhibited at low concentrations of chloramphenicol and, to a much lesser degree, gentamicin. Treating E. coli C wild type with ΦX174 and chloramphenicol eliminates the emergence of mutants with the deep rough phenotype, and thereby slows the evolution of resistance to phage infection. At slightly lower chloramphenicol concentrations, phage resistance rates are similar to those observed at high concentrations; yet, we show that the diversity of possible mutants is much larger than at higher chloramphenicol concentrations. These data suggest that specific antibiotic concentrations can lead to synergistic phage-antibiotic interactions that disappear at higher antibiotic concentrations. Overall, we show that the change in survival of various ΦX174-resistant E. coli C mutants in the presence of antibiotics can explain the observed phage-antibiotic synergism.

MeSH terms

  • Anti-Bacterial Agents* / pharmacology
  • Bacteriophage phi X 174 / drug effects
  • Bacteriophage phi X 174 / genetics
  • Chloramphenicol* / pharmacology
  • Escherichia coli* / drug effects
  • Escherichia coli* / genetics
  • Escherichia coli* / virology
  • Gentamicins* / pharmacology
  • Lipopolysaccharides* / pharmacology
  • Mutation* / genetics

Substances

  • Chloramphenicol
  • Gentamicins
  • Lipopolysaccharides
  • Anti-Bacterial Agents

Grants and funding

This work was generously supported by funds from the Max Planck Society (L.P.-F.B.). L.P. was supported by the International Max Planck Research School for Evolutionary Biology (IMPRS EvolBio). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.