Isolation and characterization of two novel groups of Kanamycin-resistance ColE1-like plasmids in Salmonella enterica serotypes from food animals

Authors: Chen, Chinyi; Strobaugh Jr, Terence; Nguyen, Ly Huong; Abley, Melanie; Lindsey, Rebecca; Jackson, Charlene

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/9/2018
Publication Date: 3/7/2018
Citation: Chen, C., Strobaugh Jr, T.P., Nguyen, L.T., Abley, M.J., Lindsey, R.L., Jackson, C.R. 2018. Isolation and characterization of two novel groups of Kanamycin-resistance ColE1-like plasmids in Salmonella enterica serotypes from food animals. PLoS One. https://doi.org/10.1371/journal.pone.0193435.
DOI: https://doi.org/10.1371/journal.pone.0193435

Interpretive Summary: Antibiotic resistant foodborne pathogens increase the burden of disease treatment and economical loss, and thus pose serious public health concerns. The problem is worsened by the ability of resistance genes to transfer among bacteria on plasmids (non-chromosomal circular DNA). In this study, small plasmids from Salmonella strains recovered from slaughter samples were characterized. A family of small plasmids in Salmonella were found to carry resistance gene(s) to kanamycin and were widely distributed among different Salmonella serotypes, with some previously not known to harbor the plasmid family. This data will improve our understanding of the distribution and occurrence of these plasmids within the Salmonella strains and reinforce the importance of more comprehensive surveillance and testing of resistant pathogens and resistance genes.

Technical Abstract: While antimicrobial resistance in Salmonella enterica is largely attributed to large plasmids, small plasmids may also harbor antimicrobial resistance genes. Previously, three major groups of ColE1-like plasmids conferring kanamycin-resistance (KanR) in various S. enterica serotypes from diagnostic samples of human or animals were reported. In this study, over 200 KanR S. enterica isolates from slaughter samples, collected in 2010 and 2011 as a part of the animal arm of the National Antimicrobial Resistance Monitoring System, were screened for the presence of ColE1-like plasmids. Twenty-three KanR ColE1-like plasmids were successfully isolated. Restriction fragment mapping revealed five major plasmid groups with subgroups, including two new groups X (n=3) and Y/Y2/Y3 (n=4), in addition to the previously identified groups A (n=7), B (n=6), and C/C3 (n=3). Nearly 75% of the plasmid-carrying isolates were from turkey and included all the isolates carrying X and Y plasmids. All group X plasmids were from serotype Hadar. Serotype Senftenberg carried all the group Y plasmids and one group B plasmid. All Typhimurium isolates (n=4) carried group A plasmids, while Newport isolates (n=3) each carried a different plasmid group (A, B, or C). This study demonstrated that KanR ColE1-like plasmids are widely distributed among different Salmonella serotypes and may play a role in dissemination of antimicrobial resistance genes. IMPORTANCE It is critical to understand the diversity of mobile genetic elements and the resistance genes that they harbor in order to combat the ever-increasing problems of antibiotic resistance. Conventionally most studies on antibiotic resistance are focused on large plasmids or chromosomal elements while research on small plasmids carrying resistance gene(s) is scarce. In this study, over 200 Salmonella isolates from slaughter samples were screened for the presence of small ColE1-like plasmids responsible for dissemination of kanamycin resistance (KanR). Approximately 10% of the screened isolates harbored KanR ColE1-like plasmids. These plasmids were further analyzed and revealed new patterns that have not been previously identified, suggesting that they may be more diverse among isolates from different sample sources and serotypes. This study underscored the importance of more comprehensive surveillance and monitoring to cover the neglected area of small plasmids carrying resistance genes.