Whole-genome sequencing and phylogenetic analysis capture the emergence of a multi-drug resistant Salmonella enterica serovar Infantis clone from diagnostic animal samples in the United States

Mariela E Srednik; Brenda R Morningstar-Shaw; Jessica A Hicks; Christopher Tong; Tonya A Mackie; Linda K Schlater

doi:10.3389/fmicb.2023.1166908

Whole-genome sequencing and phylogenetic analysis capture the emergence of a multi-drug resistant Salmonella enterica serovar Infantis clone from diagnostic animal samples in the United States

Front Microbiol. 2023 Jun 2:14:1166908. doi: 10.3389/fmicb.2023.1166908. eCollection 2023.

Authors

Mariela E Srednik¹, Brenda R Morningstar-Shaw¹, Jessica A Hicks¹, Christopher Tong², Tonya A Mackie¹, Linda K Schlater¹

Affiliations

¹ National Veterinary Services Laboratories, Animal and Plant Health Inspection Service, U.S. Department of Agriculture, Ames, IA, United States.
² Center for Veterinary Biologics, Animal and Plant Health Inspection Service, U.S. Department of Agriculture, Ames, IA, United States.

Abstract

Introduction: Salmonella enterica is a major cause of foodborne illness in the United States. A multi-drug resistant (MDR) emergent Salmonella Infantis (ESI) with a megaplasmid (pESI) was first identified in Israel and Italy and subsequently reported worldwide. The ESI clone carrying an extended spectrum β-lactamase blaCTX-M-65 on a pESI-like plasmid and a mutation in the gyrA gene has recently been found in the United States in poultry meat.

Methods: We analyzed the phenotypic and genotypic antimicrobial resistance, genomics and phylogeny of 200 S. infantis isolates from animal diagnostic samples.

Results: Of these, 33.5% were resistant to at least one antimicrobial and 19.5% were multi-drug resistant (MDR). Eleven isolates from different animal sources were phenotypically and genetically similar to the ESI clone. These isolates had a D87Y mutation in the gyrA gene conferring reduced susceptibility to ciprofloxacin and harbored a combination of 6-10 resistance genes: blaCTX-M-65, aac(3)-IVa, aadA1, aph(4)-Ia, aph(3')-Ia, floR, sul1, dfrA14, tetA, and fosA. These 11 isolates carried class I and class II integrons and three virulence genes: sinH, involved in adhesion and invasion, ybtQ and ybtP, associated with iron transport. These isolates were also closely related to each other (separated by 7 to 27 SNPs) and phylogenetically related to the ESI clone recently found in the U.S.

Discussion: This dataset captured the emergence of the MDR ESI clone in multiple animal species and the first report of a pESI-like plasmid in isolates from horses in the U.S.

Keywords: Salmonella Infantis; antimicrobial resistance; extended spectrum beta-lactamases; integron (intI1 and intI2); megaplasmids; pESI- like; phylogeny; whole genome sequencing.