Clustered Regularly Interspaced Short Palindromic Repeats Genotyping of Multidrug-Resistant Salmonella Heidelberg Strains Isolated From the Poultry Production Chain Across Brazil

Detalhes bibliográficos
Autor(a) principal: Monte, Daniel F. M. [UNESP]
Data de Publicação: 2022
Outros Autores: Nethery, Matthew A., Berman, Hanna, Keelara, Shivaramu, Lincopan, Nilton, Fedorka-Cray, Paula J., Barrangou, Rodolphe, Landgraf, Mariza
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.3389/fmicb.2022.867278
http://hdl.handle.net/11449/241287
Resumo: Salmonella enterica subsp. enterica serovar Heidelberg has been associated with a broad host range, such as poultry, dairy calves, swine, wild birds, environment, and humans. The continuous evolution of S. Heidelberg raises a public health concern since there is a global dispersal of lineages harboring a wide resistome and virulome on a global scale. Here, we characterized the resistome, phylogenetic structure and clustered regularly interspaced short palindromic repeats (CRISPR) array composition of 81 S. Heidelberg strains isolated from broiler farms (n = 16), transport and lairage (n = 5), slaughterhouse (n = 22), and retail market (n = 38) of the poultry production chain in Brazil, between 2015 and 2016 using high-resolution approaches including whole-genome sequencing (WGS) and WGS-derived CRISPR genotyping. More than 91% of the S. Heidelberg strains were multidrug-resistant. The total antimicrobial resistance (AMR) gene abundances did not vary significantly across regions and sources suggesting the widespread distribution of antibiotic-resistant strains from farm to market. The highest AMR gene abundance was observed for fosA7, aac(6′)-Iaa, sul2, tet(A), gyrA, and parC for 100% of the isolates, followed by 88.8% for blaCMY–2. The β-lactam resistance was essentially driven by the presence of the plasmid-mediated AmpC (pAmpC) blaCMY–2 gene, given the isolates which did not carry this gene were susceptible to cefoxitin (FOX). Most S. Heidelberg strains were classified within international lineages, which were phylogenetically nested with Salmonella strains from European countries; while CRISPR genotyping analysis revealed that the spacer content was overall highly conserved, but distributed into 13 distinct groups. In summary, our findings underscore the potential role of S. Heidelberg as a key pathogen disseminated from farm to fork in Brazil and reinforce the importance of CRISPR-based genotyping for salmonellae. Hence, we emphasized the need for continuous mitigation programs to monitor the dissemination of this high-priority pathogen.
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spelling Clustered Regularly Interspaced Short Palindromic Repeats Genotyping of Multidrug-Resistant Salmonella Heidelberg Strains Isolated From the Poultry Production Chain Across Brazilantibiotic resistanceCRISPRfoodborne diseasephylogenySalmonella HeidelbergWGSSalmonella enterica subsp. enterica serovar Heidelberg has been associated with a broad host range, such as poultry, dairy calves, swine, wild birds, environment, and humans. The continuous evolution of S. Heidelberg raises a public health concern since there is a global dispersal of lineages harboring a wide resistome and virulome on a global scale. Here, we characterized the resistome, phylogenetic structure and clustered regularly interspaced short palindromic repeats (CRISPR) array composition of 81 S. Heidelberg strains isolated from broiler farms (n = 16), transport and lairage (n = 5), slaughterhouse (n = 22), and retail market (n = 38) of the poultry production chain in Brazil, between 2015 and 2016 using high-resolution approaches including whole-genome sequencing (WGS) and WGS-derived CRISPR genotyping. More than 91% of the S. Heidelberg strains were multidrug-resistant. The total antimicrobial resistance (AMR) gene abundances did not vary significantly across regions and sources suggesting the widespread distribution of antibiotic-resistant strains from farm to market. The highest AMR gene abundance was observed for fosA7, aac(6′)-Iaa, sul2, tet(A), gyrA, and parC for 100% of the isolates, followed by 88.8% for blaCMY–2. The β-lactam resistance was essentially driven by the presence of the plasmid-mediated AmpC (pAmpC) blaCMY–2 gene, given the isolates which did not carry this gene were susceptible to cefoxitin (FOX). Most S. Heidelberg strains were classified within international lineages, which were phylogenetically nested with Salmonella strains from European countries; while CRISPR genotyping analysis revealed that the spacer content was overall highly conserved, but distributed into 13 distinct groups. In summary, our findings underscore the potential role of S. Heidelberg as a key pathogen disseminated from farm to fork in Brazil and reinforce the importance of CRISPR-based genotyping for salmonellae. Hence, we emphasized the need for continuous mitigation programs to monitor the dissemination of this high-priority pathogen.Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Department of Food and Experimental Nutrition Faculty of Pharmaceutical Sciences Food Research Center University of São PauloLaboratory of Avian Pathology Department of Pathology Theriogenology and One Health São Paulo State University (FCAV-Unesp)Genomic Sciences Graduate Program North Carolina State UniversityDepartment of Food Bioprocessing and Nutrition Sciences North Carolina State UniversityDepartment of Population Health and Pathobiology College of Veterinary Medicine North Carolina State UniversityDepartment of Microbiology Institute of Biomedical Sciences University of São PauloDepartment of Clinical Analysis Faculty of Pharmaceutical Sciences University of São PauloLaboratory of Avian Pathology Department of Pathology Theriogenology and One Health São Paulo State University (FCAV-Unesp)FAPESP: FoRC-2013/07914-8Universidade de São Paulo (USP)Universidade Estadual Paulista (UNESP)North Carolina State UniversityMonte, Daniel F. M. [UNESP]Nethery, Matthew A.Berman, HannaKeelara, ShivaramuLincopan, NiltonFedorka-Cray, Paula J.Barrangou, RodolpheLandgraf, Mariza2023-03-01T20:55:14Z2023-03-01T20:55:14Z2022-06-17info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.3389/fmicb.2022.867278Frontiers in Microbiology, v. 13.1664-302Xhttp://hdl.handle.net/11449/24128710.3389/fmicb.2022.8672782-s2.0-85133601322Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengFrontiers in Microbiologyinfo:eu-repo/semantics/openAccess2024-06-07T13:02:49Zoai:repositorio.unesp.br:11449/241287Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T21:29:10.153082Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Clustered Regularly Interspaced Short Palindromic Repeats Genotyping of Multidrug-Resistant Salmonella Heidelberg Strains Isolated From the Poultry Production Chain Across Brazil
title Clustered Regularly Interspaced Short Palindromic Repeats Genotyping of Multidrug-Resistant Salmonella Heidelberg Strains Isolated From the Poultry Production Chain Across Brazil
spellingShingle Clustered Regularly Interspaced Short Palindromic Repeats Genotyping of Multidrug-Resistant Salmonella Heidelberg Strains Isolated From the Poultry Production Chain Across Brazil
Monte, Daniel F. M. [UNESP]
antibiotic resistance
CRISPR
foodborne disease
phylogeny
Salmonella Heidelberg
WGS
title_short Clustered Regularly Interspaced Short Palindromic Repeats Genotyping of Multidrug-Resistant Salmonella Heidelberg Strains Isolated From the Poultry Production Chain Across Brazil
title_full Clustered Regularly Interspaced Short Palindromic Repeats Genotyping of Multidrug-Resistant Salmonella Heidelberg Strains Isolated From the Poultry Production Chain Across Brazil
title_fullStr Clustered Regularly Interspaced Short Palindromic Repeats Genotyping of Multidrug-Resistant Salmonella Heidelberg Strains Isolated From the Poultry Production Chain Across Brazil
title_full_unstemmed Clustered Regularly Interspaced Short Palindromic Repeats Genotyping of Multidrug-Resistant Salmonella Heidelberg Strains Isolated From the Poultry Production Chain Across Brazil
title_sort Clustered Regularly Interspaced Short Palindromic Repeats Genotyping of Multidrug-Resistant Salmonella Heidelberg Strains Isolated From the Poultry Production Chain Across Brazil
author Monte, Daniel F. M. [UNESP]
author_facet Monte, Daniel F. M. [UNESP]
Nethery, Matthew A.
Berman, Hanna
Keelara, Shivaramu
Lincopan, Nilton
Fedorka-Cray, Paula J.
Barrangou, Rodolphe
Landgraf, Mariza
author_role author
author2 Nethery, Matthew A.
Berman, Hanna
Keelara, Shivaramu
Lincopan, Nilton
Fedorka-Cray, Paula J.
Barrangou, Rodolphe
Landgraf, Mariza
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidade de São Paulo (USP)
Universidade Estadual Paulista (UNESP)
North Carolina State University
dc.contributor.author.fl_str_mv Monte, Daniel F. M. [UNESP]
Nethery, Matthew A.
Berman, Hanna
Keelara, Shivaramu
Lincopan, Nilton
Fedorka-Cray, Paula J.
Barrangou, Rodolphe
Landgraf, Mariza
dc.subject.por.fl_str_mv antibiotic resistance
CRISPR
foodborne disease
phylogeny
Salmonella Heidelberg
WGS
topic antibiotic resistance
CRISPR
foodborne disease
phylogeny
Salmonella Heidelberg
WGS
description Salmonella enterica subsp. enterica serovar Heidelberg has been associated with a broad host range, such as poultry, dairy calves, swine, wild birds, environment, and humans. The continuous evolution of S. Heidelberg raises a public health concern since there is a global dispersal of lineages harboring a wide resistome and virulome on a global scale. Here, we characterized the resistome, phylogenetic structure and clustered regularly interspaced short palindromic repeats (CRISPR) array composition of 81 S. Heidelberg strains isolated from broiler farms (n = 16), transport and lairage (n = 5), slaughterhouse (n = 22), and retail market (n = 38) of the poultry production chain in Brazil, between 2015 and 2016 using high-resolution approaches including whole-genome sequencing (WGS) and WGS-derived CRISPR genotyping. More than 91% of the S. Heidelberg strains were multidrug-resistant. The total antimicrobial resistance (AMR) gene abundances did not vary significantly across regions and sources suggesting the widespread distribution of antibiotic-resistant strains from farm to market. The highest AMR gene abundance was observed for fosA7, aac(6′)-Iaa, sul2, tet(A), gyrA, and parC for 100% of the isolates, followed by 88.8% for blaCMY–2. The β-lactam resistance was essentially driven by the presence of the plasmid-mediated AmpC (pAmpC) blaCMY–2 gene, given the isolates which did not carry this gene were susceptible to cefoxitin (FOX). Most S. Heidelberg strains were classified within international lineages, which were phylogenetically nested with Salmonella strains from European countries; while CRISPR genotyping analysis revealed that the spacer content was overall highly conserved, but distributed into 13 distinct groups. In summary, our findings underscore the potential role of S. Heidelberg as a key pathogen disseminated from farm to fork in Brazil and reinforce the importance of CRISPR-based genotyping for salmonellae. Hence, we emphasized the need for continuous mitigation programs to monitor the dissemination of this high-priority pathogen.
publishDate 2022
dc.date.none.fl_str_mv 2022-06-17
2023-03-01T20:55:14Z
2023-03-01T20:55:14Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.3389/fmicb.2022.867278
Frontiers in Microbiology, v. 13.
1664-302X
http://hdl.handle.net/11449/241287
10.3389/fmicb.2022.867278
2-s2.0-85133601322
url http://dx.doi.org/10.3389/fmicb.2022.867278
http://hdl.handle.net/11449/241287
identifier_str_mv Frontiers in Microbiology, v. 13.
1664-302X
10.3389/fmicb.2022.867278
2-s2.0-85133601322
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Frontiers in Microbiology
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
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