Carriage and gene content variability of the pESI-like plasmid associated with Salmonella Infantis recently established in United States poultry production

Authors: McMillan, Elizabeth; Frye, Jonathan; Jackson, Charlene; WASILENKO, JAMIE - Food Safety Inspection Service (FSIS); TAGG, KAITLIN - Centers For Disease Control And Prevention (CDC) - United States; CHEN, JESSICA - Centers For Disease Control And Prevention (CDC) - United States; SIMMONS, MUSTAFA - Food Safety Inspection Service (FSIS); GUPTA, SUSHIM - Oklahoma State University; TILLMAN, GLENN - Food Safety Inspection Service (FSIS); FOLSTER, JASON - Centers For Disease Control And Prevention (CDC) - United States

Submitted to: Genes
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/16/2020
Publication Date: 12/18/2020
Citation: Mcmillan, E.A., Frye, J.G., Jackson, C.R., Wasilenko, J.L., Tagg, K.A., Chen, J.C., Simmons, M., Gupta, S.K., Tillman, G.E., Folster, J. 2020. Carriage and gene content variability of the pESI-like plasmid associated with Salmonella Infantis recently established in United States poultry production. Genes. 11(12):1516. https://doi.org/10.3390/genes11121516.
DOI: https://doi.org/10.3390/genes11121516

Interpretive Summary: Salmonella is a common cause of foodborne illness in the United States. Salmonella serotype Infantis carrying a blaCTX-M-65 gene which makes it resistant to extended spectrum beta-lactam antibiotics, such as ceftriaxone, has recently emerged in the U.S. poultry industry and around the world. These antibiotics are used to treat Salmonella infections; therefore, the increase in antibiotic resistant Salmonella from poultry is concerning. This antibiotic resistance gene is carried by the large plasmid, pESI (plasmid for emerging Salmonella Infantis). To help understand this problem, Salmonella isolates from humans and animals in the U.S. that carry this plasmid was estimated. Function, diversity, and presence of other genes on this plasmid in Salmonella Infantis from the U.S. and around the world was also determined. Using whole genome sequences of Salmonella collected by the Food Safety and Inspection Service (FSIS) and the Centers for Disease Control and Prevention (CDC), 654 isolates collected by FSIS and 56 collected by CDC that contained the plasmid were found; all were serotype Infantis. However, only 49% of the FSIS plasmids and 66% the CDC plasmids contained the blaCTX-M-65 gene. Also, while only 61% of plasmids contained the blaCTX-M-65 gene, greater than 90% contained other genes that would help the bacteria survive better in a poultry host. Additionally, the majority of plasmids contained similar genes regardless of source. From this data, it was concluded that the number of Salmonella Infantis isolates that contain this plasmid in the U.S. is increasing, and there are likely two different lineages of the plasmid. This information will allow poultry producers to modify how they grow and process chickens to remove conditions that give Salmonella with the pESI plasmid an advantage and thus selects for resistance to extended spectrum beta-lactam resistance.

Technical Abstract: Salmonella Infantis carrying Extended Spectrum ß-Lactamase blaCTX-M-65 on a pESI-like megaplasmid has recently emerged in United States poultry. In order to determine the carriage rate and gene content variability of this plasmid in the U.S., Salmonella whole genome sequencing data containing the pESI-like plasmid isolated from humans and animals in the U.S. and internationally were analyzed. U.S. Department of Agriculture Food Safety and Inspection Service collected 654 product sampling isolates through verification testing containing pESI-like plasmids between 2017 and 2018. The Centers for Disease Control and Prevention collected 56 isolates with pESI-like plasmids between 2016 and 2018 through the National Antimicrobial Resistance Monitoring System. Approximately 49% of pESI-like plasmids from FSIS product sampling isolates and 66% of those collected by CDC contained blaCTX-M-65. Pangenome analysis was performed using Roary. All plasmids contained traN and more than 95% of plasmids contained 172 other conserved genes; approximately 61% contained blaCTX-M-65. In a hierarchal clustering analysis, some plasmids from U.S. animal sources clustered together and some plasmids from South America clustered together, possibly indicating multiple plasmid lineages. However, most plasmids contained similar genes regardless of origin. Carriage of the pESI-like plasmid in U.S. Infantis isolates appears to be increasing over time.