Bacteriophages Isolated from Chicken Meat and the Horizontal Transfer of Antimicrobial Resistance Genes

Abstract

Antimicrobial resistance in microbes poses a global and increasing threat to public health. The horizontal transfer of antimicrobial resistance genes was thought to be due largely to conjugative plasmids or transposons, with only a minor part being played by transduction through bacteriophages. However, whole-genome sequencing has recently shown that the latter mechanism could be highly important in the exchange of antimicrobial resistance genes between microorganisms and environments. The transfer of antimicrobial resistance genes by phages could underlie the origin of resistant bacteria found in food. We show that chicken meat carries a number of phages capable of transferring antimicrobial resistance. Of 243 phages randomly isolated from chicken meat, about a quarter (24.7%) were able to transduce resistance to one or more of the five antimicrobials tested into Escherichia coli ATCC 13706 (DSM 12242). Resistance to kanamycin was transduced the most often, followed by that to chloramphenicol, with four phages transducing tetracycline resistance and three transducing ampicillin resistance. Phages able to transduce antimicrobial resistance were isolated from 44% of the samples of chicken meat that we tested. The statistically significant (P = 0.01) relationship between the presence of phages transducing kanamycin resistance and E. coli isolates resistant to this antibiotic suggests that transduction may be an important mechanism for transferring kanamycin resistance to E. coli. It appears that the transduction of resistance to certain antimicrobials, e.g., kanamycin, not only is widely distributed in E. coli isolates found on meat but also could represent a major mechanism for resistance transfer. The result is of high importance for animal and human health.

FIG 1

Proportion of resistance-transducing phages among all isolated phages. Kanamycin resistance-transducing phages were detected the most often (n = 43 of 243 phages detected), followed by chloramphenicol (n = 8) and tetracycline (n = 4) resistance-transducing phages. Three phages were found to transduce kanamycin plus ampicillin resistance, and two phages transduced kanamycin plus chloramphenicol resistance. ϕCm^r, ϕKm^r, ϕTet^r, ϕKm^r Amp^r, and ϕKm^r Cm^r, chloramphenicol, kanamycin, tetracycline, kanamycin and ampicillin, and kanamycin and chloramphenicol resistance-transducing phages, respectively.