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Title: Natural Horizontal Gene Transfer of Antimicrobial Resistance Genes in Campylobacter spp. From Turkeys and Swine

Abstract

Antibiotic-resistant Campylobacter constitutes a serious threat to public health. The clonal expansion of resistant strains and/or the horizontal spread of resistance genes to other strains and species can hinder the clinical effectiveness of antibiotics to treat severe campylobacteriosis. Still, gaps exist in our understanding of the risks of acquisition and spread of antibiotic resistance in Campylobacter. While the in vitro transfer of antimicrobial resistance genes between Campylobacter species via natural transformation has been extensively demonstrated, experimental studies have favored the use of naked DNA to obtain transformants. In this study, we used experimental designs closer to real-world conditions to evaluate the possible transfer of antimicrobial resistance genes between Campylobacter strains of the same or different species (Campylobacter coli or Campylobacter jejuni) and originating from different animal hosts (swine or turkeys). This was evaluated in vitro through co-culture experiments and in vivo with dual-strain inoculation of turkeys, followed by whole genome sequencing of parental and newly emerged strains. In vitro, we observed four independent horizontal gene transfer events leading to the acquisition of resistance to beta-lactams (blaOXA), aminoglycosides [aph(2")-If and rpsL] and tetracycline [tet(O)]. Observed events involved the displacement of resistance-associated genes by a mutated version, or the acquisition of genomicmore » islands harboring a resistance determinant by homologous recombination; we did not detect the transfer of resistance-carrying plasmids even though they were present in some strains. In vivo, we recovered a newly emerged strain with dual-resistance pattern and identified the replacement of an existing non-functional tet(O) by a functional tet(O) in the recipient strain. Whole genome comparisons allowed characterization of the events involved in the horizontal spread of resistance genes between Campylobacter following in vitro co-culture and in vivo dual inoculation. Our study also highlights the potential for antimicrobial resistance transfer across Campylobacter species originating from turkeys and swine, which may have implications for farms hosting both species in close proximity.« less

Authors:
 [1];  [2];  [3];  [4];  [2];  [5];  [5];  [2]
+ Show Author Affiliations
  1. National Animal Disease Center, Ames, IA (United States); Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)
  2. National Animal Disease Center, Ames, IA (United States)
  3. National Animal Disease Center, Ames, IA (United States); Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States); Iowa State University, Ames, IA (United States)
  4. Shandong Academy of Agricultural Sciences, Jinan (China)
  5. North Carolina State University, Raleigh, NC (United States)
Publication Date:
Research Org.:
Oak Ridge Inst. for Science and Education (ORISE), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC); US Department of Agriculture (USDA)
OSTI Identifier:
1904958
Grant/Contract Number:  
SC0014664
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 12; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; antimicrobial resistance; Campylobacter; transformation; turkey; swine; animal experiment; co-culture experiment; horizontal gene transfer

Citation Formats

Guernier-Cambert, Vanina, Trachsel, Julian, Maki, Joel, Qi, Jing, Sylte, Matthew J., Hanafy, Zahra, Kathariou, Sophia, and Looft, Torey. Natural Horizontal Gene Transfer of Antimicrobial Resistance Genes in Campylobacter spp. From Turkeys and Swine. United States: N. p., 2021. Web. doi:10.3389/fmicb.2021.732969.
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Guernier-Cambert, Vanina, Trachsel, Julian, Maki, Joel, Qi, Jing, Sylte, Matthew J., Hanafy, Zahra, Kathariou, Sophia, & Looft, Torey. Natural Horizontal Gene Transfer of Antimicrobial Resistance Genes in Campylobacter spp. From Turkeys and Swine. United States. https://doi.org/10.3389/fmicb.2021.732969
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Guernier-Cambert, Vanina, Trachsel, Julian, Maki, Joel, Qi, Jing, Sylte, Matthew J., Hanafy, Zahra, Kathariou, Sophia, and Looft, Torey. Mon . "Natural Horizontal Gene Transfer of Antimicrobial Resistance Genes in Campylobacter spp. From Turkeys and Swine". United States. https://doi.org/10.3389/fmicb.2021.732969. https://www.osti.gov/servlets/purl/1904958.
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@article{osti_1904958,
title = {Natural Horizontal Gene Transfer of Antimicrobial Resistance Genes in Campylobacter spp. From Turkeys and Swine},
author = {Guernier-Cambert, Vanina and Trachsel, Julian and Maki, Joel and Qi, Jing and Sylte, Matthew J. and Hanafy, Zahra and Kathariou, Sophia and Looft, Torey},
abstractNote = {Antibiotic-resistant Campylobacter constitutes a serious threat to public health. The clonal expansion of resistant strains and/or the horizontal spread of resistance genes to other strains and species can hinder the clinical effectiveness of antibiotics to treat severe campylobacteriosis. Still, gaps exist in our understanding of the risks of acquisition and spread of antibiotic resistance in Campylobacter. While the in vitro transfer of antimicrobial resistance genes between Campylobacter species via natural transformation has been extensively demonstrated, experimental studies have favored the use of naked DNA to obtain transformants. In this study, we used experimental designs closer to real-world conditions to evaluate the possible transfer of antimicrobial resistance genes between Campylobacter strains of the same or different species (Campylobacter coli or Campylobacter jejuni) and originating from different animal hosts (swine or turkeys). This was evaluated in vitro through co-culture experiments and in vivo with dual-strain inoculation of turkeys, followed by whole genome sequencing of parental and newly emerged strains. In vitro, we observed four independent horizontal gene transfer events leading to the acquisition of resistance to beta-lactams (blaOXA), aminoglycosides [aph(2")-If and rpsL] and tetracycline [tet(O)]. Observed events involved the displacement of resistance-associated genes by a mutated version, or the acquisition of genomic islands harboring a resistance determinant by homologous recombination; we did not detect the transfer of resistance-carrying plasmids even though they were present in some strains. In vivo, we recovered a newly emerged strain with dual-resistance pattern and identified the replacement of an existing non-functional tet(O) by a functional tet(O) in the recipient strain. Whole genome comparisons allowed characterization of the events involved in the horizontal spread of resistance genes between Campylobacter following in vitro co-culture and in vivo dual inoculation. Our study also highlights the potential for antimicrobial resistance transfer across Campylobacter species originating from turkeys and swine, which may have implications for farms hosting both species in close proximity.},
doi = {10.3389/fmicb.2021.732969},
journal = {Frontiers in Microbiology},
number = ,
volume = 12,
place = {United States},
year = {Mon Sep 27 00:00:00 EDT 2021},
month = {Mon Sep 27 00:00:00 EDT 2021}
}
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https://doi.org/10.3389/fmicb.2021.732969
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