A single nucleotide change in mutY increases the emergence of antibiotic-resistant Campylobacter jejuni mutants

J Antimicrob Chemother. 2015 Oct;70(10):2739-48. doi: 10.1093/jac/dkv190. Epub 2015 Jul 13.

Abstract

Objectives: Mutator strains play an important role in the emergence of antibiotic-resistant bacteria. Campylobacter jejuni is a leading cause of foodborne illnesses worldwide and is increasingly resistant to clinically important antibiotics. The objective of this study was to identify the genetic basis that contributes to a mutator phenotype in Campylobacter and determine the role of this phenotype in the development of antibiotic resistance.

Methods: A C. jejuni isolate (named CMT) showing a mutator phenotype was subjected to WGS analysis. Comparative genomics, site-specific reversion and mutation, and gene knockout were conducted to prove the mutator effect was caused by a single nucleotide change in the mutY gene of C. jejuni.

Results: The C. jejuni CMT isolate showed ∼ 100-fold higher mutation frequency to ciprofloxacin than the WT strain. Under selection by ciprofloxacin, fluoroquinolone-resistant mutants emerged readily from the CMT isolate. WGS identified a single nucleotide change (G595 → T) in the mutY gene of the CMT isolate. Further experiments using defined mutant constructs proved its specific role in elevating mutation frequencies. The mutY point mutation also led to an ∼ 700-fold increase in the emergence of ampicillin-resistant mutants, indicating its broader impact on antibiotic resistance. Structural modelling suggested the G595 → T mutation probably affects the catalytic domain of MutY and consequently abolishes the anti-mutator function of this DNA repair protein.

Conclusions: The G595 → T mutation in mutY abolishes its anti-mutator function and confers a mutator phenotype in Campylobacter, promoting the emergence of antibiotic-resistant Campylobacter.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Anti-Bacterial Agents / pharmacology
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics*
  • Campylobacter Infections / microbiology*
  • Campylobacter jejuni / drug effects*
  • Campylobacter jejuni / genetics*
  • Catalytic Domain / genetics
  • Ciprofloxacin / pharmacology
  • DNA Glycosylases / chemistry
  • DNA Glycosylases / genetics*
  • Drug Resistance, Bacterial*
  • Genome, Bacterial
  • Genomics
  • Humans
  • Microbial Sensitivity Tests
  • Mutation Rate
  • Mutation*
  • Polymorphism, Single Nucleotide*

Substances

  • Anti-Bacterial Agents
  • Bacterial Proteins
  • Ciprofloxacin
  • DNA Glycosylases