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

Abstract

c 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.

Abundance of Antibiotic Resistance Genes in Bacteriophage following Soil Fertilization with Dairy Manure or Municipal Biosolids, and Evidence for Potential Transduction

“…For instance, retail chicken meat carries a number of phage capable of transferring antimicrobial resistance; of 243 phage randomly isolated from chicken meat, about 25% was able to transduce into E. coli resistance to 1 or more of the 35 antimicrobials tested (29). Based on factors like phage versus bacterial abundance, the number of phage in a transduction-competent state, and the physical conditions of various environments, Muniesa et al (8) concluded that phage-mediated horizontal transfer between intestinal bacteria or between intestinal and indigenous bacteria in extraintestinal environments was probable.…”

“…(29) observed that of 243 bacteriophage randomly isolated from chicken meat, about a quarter was able to transduce resistance to one or more of the five antibiotics tested into E. coli.…”

Bacteriophages: Practical Applications for Nature's Biocontrol

“…This is evident in the study of Modi et al (2013) who recently revealed that the viral metagenome (or virome) of antibiotic-treated mice was highly enriched for ARGs compared with that of non-treated control mice. However, the contribution of phages to the spread of ARGs suggests that phages may play a more significant role in the emergence and spread of ARGs than previously expected (Parsley et al 2010;Colomer-Lluch et al 2011aBalcazar 2014;Marti et al 2014b;Shousha et al 2015). These findings clearly show that phages have significant implications for the emergence and spread of antibiotic resistance.…”

“…The role of phage in transduction and horizontal transfer is assumed (Christie et al 2012). This assumption recently has been confirmed by Shousha et al (2015). They demonstrate that lysogenic phages that infect E. coli (coliphages) are able to transduce important antimicrobial resistances in chicken meat.…”

“…The acquisition of antimicrobial resistance by phage transduction has been demonstrated in chicken meat relevant bacterial species, this mechanism in environmental settings has now been fully explored (Shousha et al 2015), whereas, the phage can transfer bacterial DNA from one host to the other in a process known as transduction. The co-existence of various resistance genes in the same plasmid or transposon results in the incidental transfer of the whole group, even if the selective pressure is directed towards a specific gene (Summers 2002).…”