Bacteriophage-Mediated Modulation of Bacterial Competition during Selective Enrichment of Campylobacter

Microbiol Spectr. 2021 Dec 22;9(3):e0170321. doi: 10.1128/Spectrum.01703-21. Epub 2021 Dec 15.

Abstract

Selective media using antimicrobial supplements generate unique microbial ecology to facilitate bacterial isolation. However, antibiotic-resistant bacteria indigenous to samples can interfere with the isolation process using selective media. Recent studies showed that extended-spectrum beta-lactamase (ESBL)-producing Escherichia coli is highly prevalent on retail raw chicken and compromises the efficacy of Campylobacter isolation because ESBL-producing E. coli are resistant to antimicrobial supplements in Campylobacter-selective media and outgrows Campylobacter. The objective of this study was to improve Campylobacter isolation by inhibiting the growth of ESBL-producing E. coli using bacteriophages (phages). The supplementation of Campylobacter-selective media with E. coli phages reduced the level of ESBL-producing E. coli during the enrichment step. When E. coli phages were combined with the antimicrobial supplements of Campylobacter-selective media, antimicrobial synergy was observed, particularly with rifampicin, an antibiotic used in Preston medium. Although the same materials (i.e., phages and selective media) were used, the sequence of combining the materials markedly influenced the inhibition of ESBL-producing E. coli and the isolation of Campylobacter. These findings indicated that the modulation of microbial competition at the enrichment step was critical to the successful isolation of fastidious bacteria and that phages can be utilized to facilitate the selective enrichment of target bacteria by inhibiting their competitive bacteria. IMPORTANCE Phages are promising antimicrobial alternatives. In this study, we first demonstrated that phages can be used to facilitate selective isolation of fastidious bacteria that are prone to be outgrown by bacterial competitors during isolation. The effectiveness of a phage-based isolation method was primarily dependent on the antimicrobial synergy between phages and antibiotics used in selective media. The same approach could be applied to the development of isolation methods for other fastidious bacteria.

Keywords: Campylobacter isolation; ESBL-producing Escherichia coli; antimicrobial synergy; bacteriophage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Bacteriophages*
  • Campylobacter / growth & development*
  • Campylobacter / isolation & purification*
  • Chickens / microbiology
  • Culture Media / chemistry
  • Drug Resistance, Multiple, Bacterial / genetics
  • Escherichia coli / genetics
  • Escherichia coli / growth & development*
  • Escherichia coli / metabolism
  • Escherichia coli / virology*
  • Food Contamination / analysis
  • Food Microbiology / methods
  • Meat / microbiology*
  • Microbial Sensitivity Tests
  • beta-Lactamases / metabolism

Substances

  • Anti-Bacterial Agents
  • Culture Media
  • beta-Lactamases