Phage-plasmid hybrids as vectors for antibiotic resistance in environmental Escherichia coli

Sci Total Environ. 2025 Jan 10:959:178157. doi: 10.1016/j.scitotenv.2024.178157. Epub 2024 Dec 26.

Abstract

This study investigated the potential role of phages in the dissemination of antimicrobial resistance genes (ARGs) and virulence factor genes (VFGs) in Escherichia coli (E. coli). A comprehensive in silico analysis of 18,410 phage sequences retrieved from the National Center for Biotechnology Information database (NCBI) revealed distinct carriage patterns for ARGs and VFGs between lytic, temperate, and chronic phage types. Notably, 57 temperate phages carried ARGs, particularly associated with multidrug and aminoglycoside resistance. Temperate phages (8.97 %, 635/7081) and chronic phages (8.09 %, 14/173) exhibited a significantly higher prevalence of VFGs (Chi-Square, p ≤ 0.05), particularly associated with exotoxin-related genes, compared to lytic phages (0.05 %, 6/11,156). This underscores the role phages play as reservoirs and potential vectors for the dissemination of ARGs and VFGs in bacteria. Our environmental E. coli isolates (n = 60) were found to carry 179 intact prophages containing polymyxin, macrolide, tetracycline, and multidrug resistance genes as well as various VFGs. This study documents the presence of phage-plasmids (P-Ps) in environmental E. coli isolates, offering new insights into horizontal gene transfer (HGT) mechanisms. Notably, the blaCTX-M-15 gene, associated with beta-lactam resistance, was identified in two P-Ps, suggesting a potentially novel route for the dissemination of beta-lactam resistance. The diverse replicon types observed in P-Ps suggest a broader integration capacity compared to traditional plasmids, potentially enabling the blaCTX-M-15 gene dissemination across diverse bacterial species. This study provides valuable insights into the multifaceted role of phages in shaping the antimicrobial resistance landscape. Further research is necessary to fully understand the intricate mechanisms underlying phage-mediated ARG and VFG dissemination.

Keywords: Antimicrobial resistance gene; Bioinformatics; Phage; Phage genomics; Phage-plasmid; Virulence factor gene.

MeSH terms

  • Anti-Bacterial Agents / pharmacology
  • Bacteriophages / genetics
  • Bacteriophages / physiology
  • Drug Resistance, Bacterial / genetics
  • Escherichia coli* / drug effects
  • Escherichia coli* / genetics
  • Plasmids* / genetics
  • Virulence Factors / genetics

Substances

  • Anti-Bacterial Agents
  • Virulence Factors