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

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 multiplemore » 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.« less

Authors:
 [1];  [2];  [3];  [2];  [2];  [4];  [4];  [5];  [2];  [2];  [2]
  1. U.S. Food and Drug Administration (FDA), Jefferson, AR (United States). National Center for Toxicological Research. Division of Microbiology; King Abdulaziz Univ., Jeddah (Saudi Arabia). College of Science. Biological Science Dept.
  2. U.S. Food and Drug Administration (FDA), Jefferson, AR (United States). National Center for Toxicological Research. Division of Microbiology
  3. U.S. Food and Drug Administration (FDA), Jefferson, AR (United States). National Center for Toxicological Research. Division of Microbiology; Univ. of Arkansas at Pine Bluff, AR (United States). Dept. of Agriculture
  4. U.S. Food and Drug Administration (FDA), Rockville, MD (United States). Center for Veterinary Medicine. Office of New Animal Drug Evaluation
  5. U.S. Food and Drug Administration (FDA), Jefferson, AR (United States). National Center for Toxicological Research. Division of Microbiology; Univ. of Arkansas at Pine Bluff, AR (United States). Dept. of Agriculture; National Research Centre, Giza (Egypt). Veterinary Research Division. Dept. of Parasitology and Animal Diseases
Publication Date:
Research Org.:
Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC); USFDA
OSTI Identifier:
1816813
Grant/Contract Number:  
SC0014664
Resource Type:
Accepted Manuscript
Journal Name:
Genes
Additional Journal Information:
Journal Volume: 11; Journal Issue: 11; Journal ID: ISSN 2073-4425
Publisher:
MDPI
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; IncFIB plasmids; S. Typhimurium; SNP tree; conjugation; persistence; Caco-2 intestinal epithelial cells

Citation Formats

Aljahdali, Nesreen H., Khajanchi, Bijay K., Weston, Kennedi, Deck, Joanna, Cox, Justin, Singh, Ruby, Gilbert, Jeffrey, Sanad, Yasser M., Han, Jing, Nayak, Rajesh, and Foley, Steven L. Genotypic and Phenotypic Characterization of Incompatibility Group FIB Positive Salmonella enterica Serovar Typhimurium Isolates from Food Animal Sources. United States: N. p., 2020. Web. doi:10.3390/genes11111307.
Aljahdali, Nesreen H., Khajanchi, Bijay K., Weston, Kennedi, Deck, Joanna, Cox, Justin, Singh, Ruby, Gilbert, Jeffrey, Sanad, Yasser M., Han, Jing, Nayak, Rajesh, & Foley, Steven L. Genotypic and Phenotypic Characterization of Incompatibility Group FIB Positive Salmonella enterica Serovar Typhimurium Isolates from Food Animal Sources. United States. https://doi.org/10.3390/genes11111307
Aljahdali, Nesreen H., Khajanchi, Bijay K., Weston, Kennedi, Deck, Joanna, Cox, Justin, Singh, Ruby, Gilbert, Jeffrey, Sanad, Yasser M., Han, Jing, Nayak, Rajesh, and Foley, Steven L. Wed . "Genotypic and Phenotypic Characterization of Incompatibility Group FIB Positive Salmonella enterica Serovar Typhimurium Isolates from Food Animal Sources". United States. https://doi.org/10.3390/genes11111307. https://www.osti.gov/servlets/purl/1816813.
@article{osti_1816813,
title = {Genotypic and Phenotypic Characterization of Incompatibility Group FIB Positive Salmonella enterica Serovar Typhimurium Isolates from Food Animal Sources},
author = {Aljahdali, Nesreen H. and Khajanchi, Bijay K. and Weston, Kennedi and Deck, Joanna and Cox, Justin and Singh, Ruby and Gilbert, Jeffrey and Sanad, Yasser M. and Han, Jing and Nayak, Rajesh and Foley, Steven L.},
abstractNote = {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.},
doi = {10.3390/genes11111307},
journal = {Genes},
number = 11,
volume = 11,
place = {United States},
year = {Wed Nov 04 00:00:00 EST 2020},
month = {Wed Nov 04 00:00:00 EST 2020}
}

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