Genetic Characteristics of Salmonella Isolates Recovered From Reused Broiler Litter Over Three Successive Flocks

Salmonella infections are a leading cause of bacterial food-borne illness worldwide. Infections are highly associated with the consumption of contaminated food, and in particular, chicken meat. The severity of Salmonella infections depends on the presence of antimicrobial resistance genes and virule...

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Main Authors: Reed Woyda, Adelumola Oladeinde, Dinku Endale, Timothy Strickland, Jodie Plumblee Lawrence, Zaid Abdo
Format: Article
Language:English
Published: Elsevier 2024-03-01
Series:Journal of Food Protection
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0362028X24000206
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author Reed Woyda
Adelumola Oladeinde
Dinku Endale
Timothy Strickland
Jodie Plumblee Lawrence
Zaid Abdo
author_facet Reed Woyda
Adelumola Oladeinde
Dinku Endale
Timothy Strickland
Jodie Plumblee Lawrence
Zaid Abdo
author_sort Reed Woyda
collection DOAJ
description Salmonella infections are a leading cause of bacterial food-borne illness worldwide. Infections are highly associated with the consumption of contaminated food, and in particular, chicken meat. The severity of Salmonella infections depends on the presence of antimicrobial resistance genes and virulence factors. While there are many studies which have investigated Salmonella strains isolated from postharvest chicken samples, there is a gap in our understanding of the genetic properties that influence the persistence of Salmonella in preharvest and in particular their makeup of antimicrobial resistance genes and virulence factors. We used whole genome sequencing and hierarchical clustering to characterize and classify the genetic diversity of Salmonella enterica isolates (n = 55) recovered from the litter of commercial broiler chicken raised in four colocated broiler houses of one integrated farm over three consecutive flocks. The chicken were raised under a newly adopted “No Antibiotics Ever” program, and copper sulfate was administered via drinking water. In-silico serovar prediction identified three S. enterica serovars: Enteritidis (n = 12), Kentucky (n = 40), and Senftenberg (n = 3). Antimicrobial susceptibility testing revealed that only one S. Kentucky isolate was resistant to streptomycin, while the remaining isolates were susceptible to all antibiotics tested. Metal resistance operons, including copper and silver, were identified chromosomally and on plasmids in serovar Senftenberg and Kentucky isolates, respectively, while serovar Enteritidis carried several virulence factors on plasmids. Serovar Kentucky isolates harboring metal resistance operons were the only Salmonella isolates recovered from the litter of third flock cohort. These results suggest that there might be environmental selection for Salmonella strains carrying plasmid-associated metal resistance and virulence genes, which could play a role in their persistence in litter.
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spelling doaj.art-3d8c5826b3ac4e729adea01040817b8f2024-03-04T04:11:57ZengElsevierJournal of Food Protection0362-028X2024-03-01873100236Genetic Characteristics of Salmonella Isolates Recovered From Reused Broiler Litter Over Three Successive FlocksReed Woyda0Adelumola Oladeinde1Dinku Endale2Timothy Strickland3Jodie Plumblee Lawrence4Zaid Abdo5Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA; Program of Cell and Molecular Biology, Colorado State University, Fort Collins, Colorado, USAU.S. National Poultry Research Center, USDA-ARS, Athens, Georgia, USA; Corresponding authors.Southeast Watershed Research, USDA, Tifton, Georgia, USASoutheast Watershed Research, USDA, Tifton, Georgia, USAU.S. National Poultry Research Center, USDA-ARS, Athens, Georgia, USADepartment of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado, USA; Program of Cell and Molecular Biology, Colorado State University, Fort Collins, Colorado, USA; Corresponding authors.Salmonella infections are a leading cause of bacterial food-borne illness worldwide. Infections are highly associated with the consumption of contaminated food, and in particular, chicken meat. The severity of Salmonella infections depends on the presence of antimicrobial resistance genes and virulence factors. While there are many studies which have investigated Salmonella strains isolated from postharvest chicken samples, there is a gap in our understanding of the genetic properties that influence the persistence of Salmonella in preharvest and in particular their makeup of antimicrobial resistance genes and virulence factors. We used whole genome sequencing and hierarchical clustering to characterize and classify the genetic diversity of Salmonella enterica isolates (n = 55) recovered from the litter of commercial broiler chicken raised in four colocated broiler houses of one integrated farm over three consecutive flocks. The chicken were raised under a newly adopted “No Antibiotics Ever” program, and copper sulfate was administered via drinking water. In-silico serovar prediction identified three S. enterica serovars: Enteritidis (n = 12), Kentucky (n = 40), and Senftenberg (n = 3). Antimicrobial susceptibility testing revealed that only one S. Kentucky isolate was resistant to streptomycin, while the remaining isolates were susceptible to all antibiotics tested. Metal resistance operons, including copper and silver, were identified chromosomally and on plasmids in serovar Senftenberg and Kentucky isolates, respectively, while serovar Enteritidis carried several virulence factors on plasmids. Serovar Kentucky isolates harboring metal resistance operons were the only Salmonella isolates recovered from the litter of third flock cohort. These results suggest that there might be environmental selection for Salmonella strains carrying plasmid-associated metal resistance and virulence genes, which could play a role in their persistence in litter.http://www.sciencedirect.com/science/article/pii/S0362028X24000206Broiler litterLitter reuseMetal resistanceSalmonellaVirulence factors
spellingShingle Reed Woyda
Adelumola Oladeinde
Dinku Endale
Timothy Strickland
Jodie Plumblee Lawrence
Zaid Abdo
Genetic Characteristics of Salmonella Isolates Recovered From Reused Broiler Litter Over Three Successive Flocks
Journal of Food Protection
Broiler litter
Litter reuse
Metal resistance
Salmonella
Virulence factors
title Genetic Characteristics of Salmonella Isolates Recovered From Reused Broiler Litter Over Three Successive Flocks
title_full Genetic Characteristics of Salmonella Isolates Recovered From Reused Broiler Litter Over Three Successive Flocks
title_fullStr Genetic Characteristics of Salmonella Isolates Recovered From Reused Broiler Litter Over Three Successive Flocks
title_full_unstemmed Genetic Characteristics of Salmonella Isolates Recovered From Reused Broiler Litter Over Three Successive Flocks
title_short Genetic Characteristics of Salmonella Isolates Recovered From Reused Broiler Litter Over Three Successive Flocks
title_sort genetic characteristics of salmonella isolates recovered from reused broiler litter over three successive flocks
topic Broiler litter
Litter reuse
Metal resistance
Salmonella
Virulence factors
url http://www.sciencedirect.com/science/article/pii/S0362028X24000206
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