Genotypic and Phenotypic Characterization of Incompatibility Group FIB Positive Salmonella enterica Serovar Typhimurium Isolates from Food Animal Sources.

Nesreen H Aljahdali,Bijay K Khajanchi,Justin Cox,Steven L Foley,Kennedi Weston,Joanna Deck,Jeffrey Gilbert,Yasser M Sanad,Rajesh Nayak,Jing Han,Ruby Singh

doi:10.3390/genes11111307

Abstract

Salmonella enterica is one of the most common bacterial foodborne pathogens in the United States, causing illnesses that range from self-limiting gastroenteritis to more severe, life threatening invasive disease. Many Salmonella strains contain plasmids that carry virulence, antimicrobial resistance, and/or transfer genes which allow them to adapt to diverse environments, and these can include incompatibility group (Inc) FIB plasmids. This study was undertaken to evaluate the genomic and phenotypic characteristics of IncFIB-positive Salmonella enterica serovar Typhimurium isolates from food animal sources, to identify their plasmid content, assess antimicrobial resistance and virulence properties, and compare their genotypic isolates with more recently isolated S. Typhimurium isolates from food animal sources. Methods: We identified 71 S. Typhimurium isolates that carried IncFIB plasmids. These isolates were subjected to whole genome sequencing and evaluated for bacteriocin production, antimicrobial susceptibility, the ability to transfer resistance plasmids, and a subset was evaluated for their ability to invade and persist in intestinal human epithelial cells. Results: Approximately 30% of isolates (n = 21) displayed bacteriocin inhibition of Escherichia coli strain J53. Bioinformatic analyses using PlasmidFinder software confirmed that all isolates contained IncFIB plasmids along with multiple other plasmid replicon types. Comparative analyses showed that all strains carried multiple antimicrobial resistance genes and virulence factors including iron acquisition genes, such as iucABCD (75%), iutA (94%), sitABCD (76%) and sitAB (100%). In 17 cases (71%), IncFIB plasmids, along with other plasmid replicon types, were able to conjugally transfer antimicrobial resistance and virulence genes to the susceptible recipient strain. For ten strains, persistence cell counts (27%) were noted to be significantly higher than invasion bacterial cell counts. When the genome sequences of the study isolates collected from 1998–2003 were compared to those published from subsequent years (2005–2018), overlapping genotypes were found, indicating the perseverance of IncFIB positive strains in food animal populations. This study confirms that IncFIB plasmids can play a potential role in disseminating antimicrobial resistance and virulence genes amongst bacteria from several food animal species.

Highlights

As one of the major causes of foodborne illnesses throughout the world, Salmonella enterica is estimated to cause approximately 1.35 million infections that result in 26,500 hospitalizations and 420 deaths per year in the United States alone [1,2]
Ninety-five percent of S. enterica infections are associated with consumption of contaminated food, and most often cause gastroenteritis that is characterized by stomach cramps, diarrhea, fever, and local infections [5]
S. enterica includes more than 2600 serovars, and the most predominant serovar causing human disease is S. enterica serovar Typhimurium, according to the Centers for Diseases Control and Prevention (CDC) [6,7]

Summary

Introduction

As one of the major causes of foodborne illnesses throughout the world, Salmonella enterica is estimated to cause approximately 1.35 million infections that result in 26,500 hospitalizations and 420 deaths per year in the United States alone [1,2]. The economic cost associated with these infections and death due to salmonellosis has been estimated to be up to 3.7 billion dollars each year due to loss of work, medical care, and quality of life lost [3,4]. Ninety-five percent of S. enterica infections are associated with consumption of contaminated food, and most often cause gastroenteritis that is characterized by stomach cramps, diarrhea, fever, and local infections [5]. S. Typhimurium is a potentially invasive bacterium causing illnesses ranging from mild gastroenteritis to enteric fever [8]. Typhimurium, which contributes to significant morbidity and mortality worldwide, can carry plasmids that have been shown to harbor antimicrobial resistance and virulence genes [11,12]

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