Cargando…
Antimicrobial Resistance Genes, Cassettes, and Plasmids Present in Salmonella enterica Associated With United States Food Animals
The ability of antimicrobial resistance (AR) to transfer, on mobile genetic elements (MGEs) between bacteria, can cause the rapid establishment of multidrug resistance (MDR) in bacteria from animals, thus creating a foodborne risk to human health. To investigate MDR and its association with plasmids...
Autores principales: | , , , , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2019
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6479191/ https://www.ncbi.nlm.nih.gov/pubmed/31057528 http://dx.doi.org/10.3389/fmicb.2019.00832 |
_version_ | 1783413297276518400 |
---|---|
author | McMillan, Elizabeth A. Gupta, Sushim K. Williams, Laura E. Jové, Thomas Hiott, Lari M. Woodley, Tiffanie A. Barrett, John B. Jackson, Charlene R. Wasilenko, Jamie L. Simmons, Mustafa Tillman, Glenn E. McClelland, Michael Frye, Jonathan G. |
author_facet | McMillan, Elizabeth A. Gupta, Sushim K. Williams, Laura E. Jové, Thomas Hiott, Lari M. Woodley, Tiffanie A. Barrett, John B. Jackson, Charlene R. Wasilenko, Jamie L. Simmons, Mustafa Tillman, Glenn E. McClelland, Michael Frye, Jonathan G. |
author_sort | McMillan, Elizabeth A. |
collection | PubMed |
description | The ability of antimicrobial resistance (AR) to transfer, on mobile genetic elements (MGEs) between bacteria, can cause the rapid establishment of multidrug resistance (MDR) in bacteria from animals, thus creating a foodborne risk to human health. To investigate MDR and its association with plasmids in Salmonella enterica, whole genome sequence (WGS) analysis was performed on 193 S. enterica isolated from sources associated with United States food animals between 1998 and 2011; 119 were resistant to at least one antibiotic tested. Isolates represented 86 serotypes and variants, as well as diverse phenotypic resistance profiles. A total of 923 AR genes and 212 plasmids were identified among the 193 strains. Every isolate contained at least one AR gene. At least one plasmid was detected in 157 isolates. Genes were identified for resistance to aminoglycosides (n = 472), β-lactams (n = 84), tetracyclines (n = 171), sulfonamides (n = 91), phenicols (n = 42), trimethoprim (n = 8), macrolides (n = 5), fosfomycin (n = 48), and rifampicin (n = 2). Plasmid replicon types detected in the isolates were A/C (n = 32), ColE (n = 76), F (n = 43), HI1 (n = 4), HI2 (n = 20), I1 (n = 62), N (n = 4), Q (n = 7), and X (n = 35). Phenotypic resistance correlated with the AR genes identified in 95.4% of cases. Most AR genes were located on plasmids, with many plasmids harboring multiple AR genes. Six antibiotic resistance cassette structures (ARCs) and one pseudo-cassette were identified. ARCs contained between one and five resistance genes (ARC1: sul2, strAB, tetAR; ARC2: aac3-iid; ARC3: aph, sph; ARC4: cmy-2; ARC5: floR; ARC6: tetB; pseudo-ARC: aadA, aac3-VIa, sul1). These ARCs were present in multiple isolates and on plasmids of multiple replicon types. To determine the current distribution and frequency of these ARCs, the public NCBI database was analyzed, including WGS data on isolates collected by the USDA Food Safety and Inspection Service (FSIS) from 2014 to 2018. ARC1, ARC4, and ARC5 were significantly associated with cattle isolates, while ARC6 was significantly associated with chicken isolates. This study revealed that a diverse group of plasmids, carrying AR genes, are responsible for the phenotypic resistance seen in Salmonella isolated from United States food animals. It was also determined that many plasmids carry similar ARCs. |
format | Online Article Text |
id | pubmed-6479191 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-64791912019-05-03 Antimicrobial Resistance Genes, Cassettes, and Plasmids Present in Salmonella enterica Associated With United States Food Animals McMillan, Elizabeth A. Gupta, Sushim K. Williams, Laura E. Jové, Thomas Hiott, Lari M. Woodley, Tiffanie A. Barrett, John B. Jackson, Charlene R. Wasilenko, Jamie L. Simmons, Mustafa Tillman, Glenn E. McClelland, Michael Frye, Jonathan G. Front Microbiol Microbiology The ability of antimicrobial resistance (AR) to transfer, on mobile genetic elements (MGEs) between bacteria, can cause the rapid establishment of multidrug resistance (MDR) in bacteria from animals, thus creating a foodborne risk to human health. To investigate MDR and its association with plasmids in Salmonella enterica, whole genome sequence (WGS) analysis was performed on 193 S. enterica isolated from sources associated with United States food animals between 1998 and 2011; 119 were resistant to at least one antibiotic tested. Isolates represented 86 serotypes and variants, as well as diverse phenotypic resistance profiles. A total of 923 AR genes and 212 plasmids were identified among the 193 strains. Every isolate contained at least one AR gene. At least one plasmid was detected in 157 isolates. Genes were identified for resistance to aminoglycosides (n = 472), β-lactams (n = 84), tetracyclines (n = 171), sulfonamides (n = 91), phenicols (n = 42), trimethoprim (n = 8), macrolides (n = 5), fosfomycin (n = 48), and rifampicin (n = 2). Plasmid replicon types detected in the isolates were A/C (n = 32), ColE (n = 76), F (n = 43), HI1 (n = 4), HI2 (n = 20), I1 (n = 62), N (n = 4), Q (n = 7), and X (n = 35). Phenotypic resistance correlated with the AR genes identified in 95.4% of cases. Most AR genes were located on plasmids, with many plasmids harboring multiple AR genes. Six antibiotic resistance cassette structures (ARCs) and one pseudo-cassette were identified. ARCs contained between one and five resistance genes (ARC1: sul2, strAB, tetAR; ARC2: aac3-iid; ARC3: aph, sph; ARC4: cmy-2; ARC5: floR; ARC6: tetB; pseudo-ARC: aadA, aac3-VIa, sul1). These ARCs were present in multiple isolates and on plasmids of multiple replicon types. To determine the current distribution and frequency of these ARCs, the public NCBI database was analyzed, including WGS data on isolates collected by the USDA Food Safety and Inspection Service (FSIS) from 2014 to 2018. ARC1, ARC4, and ARC5 were significantly associated with cattle isolates, while ARC6 was significantly associated with chicken isolates. This study revealed that a diverse group of plasmids, carrying AR genes, are responsible for the phenotypic resistance seen in Salmonella isolated from United States food animals. It was also determined that many plasmids carry similar ARCs. Frontiers Media S.A. 2019-04-17 /pmc/articles/PMC6479191/ /pubmed/31057528 http://dx.doi.org/10.3389/fmicb.2019.00832 Text en Copyright © 2019 McMillan, Gupta, Williams, Jové, Hiott, Woodley, Barrett, Jackson, Wasilenko, Simmons, Tillman, McClelland and Frye. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Microbiology McMillan, Elizabeth A. Gupta, Sushim K. Williams, Laura E. Jové, Thomas Hiott, Lari M. Woodley, Tiffanie A. Barrett, John B. Jackson, Charlene R. Wasilenko, Jamie L. Simmons, Mustafa Tillman, Glenn E. McClelland, Michael Frye, Jonathan G. Antimicrobial Resistance Genes, Cassettes, and Plasmids Present in Salmonella enterica Associated With United States Food Animals |
title | Antimicrobial Resistance Genes, Cassettes, and Plasmids Present in Salmonella enterica Associated With United States Food Animals |
title_full | Antimicrobial Resistance Genes, Cassettes, and Plasmids Present in Salmonella enterica Associated With United States Food Animals |
title_fullStr | Antimicrobial Resistance Genes, Cassettes, and Plasmids Present in Salmonella enterica Associated With United States Food Animals |
title_full_unstemmed | Antimicrobial Resistance Genes, Cassettes, and Plasmids Present in Salmonella enterica Associated With United States Food Animals |
title_short | Antimicrobial Resistance Genes, Cassettes, and Plasmids Present in Salmonella enterica Associated With United States Food Animals |
title_sort | antimicrobial resistance genes, cassettes, and plasmids present in salmonella enterica associated with united states food animals |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6479191/ https://www.ncbi.nlm.nih.gov/pubmed/31057528 http://dx.doi.org/10.3389/fmicb.2019.00832 |
work_keys_str_mv | AT mcmillanelizabetha antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals AT guptasushimk antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals AT williamslaurae antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals AT jovethomas antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals AT hiottlarim antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals AT woodleytiffaniea antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals AT barrettjohnb antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals AT jacksoncharlener antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals AT wasilenkojamiel antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals AT simmonsmustafa antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals AT tillmanglenne antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals AT mcclellandmichael antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals AT fryejonathang antimicrobialresistancegenescassettesandplasmidspresentinsalmonellaentericaassociatedwithunitedstatesfoodanimals |