Genomic Features and Phylogenetic Analysis of Antimicrobial-Resistant Salmonella Mbandaka ST413 Strains

Detalhes bibliográficos
Autor(a) principal: Benevides, Valdinete Pereira
Data de Publicação: 2024
Outros Autores: Saraiva, Mauro de Mesquita Souza, Nascimento, Camila de Fátima, Delgado-Suárez, Enrique Jesús, Oliveira, Celso José Bruno, Silva, Saura Rodrigues, Miranda, Vitor Fernandes Oliveira, Christensen, Henrik, Olsen, John Elmerdahl, Berchieri Junior, Angelo
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: https://hdl.handle.net/11449/253509
https://doi.org/10.3390/microorganisms12020312
Resumo: In recent years, Salmonella enterica subsp. enterica serovar Mbandaka (S. Mbandaka) has been increasingly isolated from laying hens and shell eggs around the world. Moreover, this serovar has been identified as the causative agent of several salmonellosis outbreaks in humans. Surprisingly, little is known about the characteristics of this emerging serovar, and therefore, we investigated antimicrobial resistance, virulence, and prophage genes of six selected Brazilian strains of Salmonella Mbandaka using Whole Genome Sequencing (WGS). Multi-locus sequence typing revealed that the tested strains belong to Sequence Type 413 (ST413), which has been linked to recent multi-country salmonellosis outbreaks in Europe. A total of nine resistance genes were detected, and the most frequent ones were aac(6′)-Iaa, sul1, qacE, blaOXA-129, tet(B), and aadA1. A point mutation in ParC at the 57th position (threonine → serine) associated with quinolone resistance was present in all investigated genomes. A 112,960 bp IncHI2A plasmid was mapped in 4/6 strains. This plasmid harboured tetracycline (tetACDR) and mercury (mer) resistance genes, genes contributing to conjugative transfer, and genes involved in plasmid maintenance. Most strains (four/six) carried Salmonella genomic island 1 (SGI1). All S. Mbandaka genomes carried seven pathogenicity islands (SPIs) involved in intracellular survival and virulence: SPIs 1-5, 9, and C63PI. The virulence genes csgC, fimY, tcfA, sscA, (two/six), and ssaS (one/six) were absent in some of the genomes; conversely, fimA, prgH, and mgtC were present in all of them. Five Salmonella bacteriophage sequences (with homology to Escherichia phage phiV10, Enterobacteria phage Fels-2, Enterobacteria phage HK542, Enterobacteria phage ST64T, Salmonella phage SW9) were identified, with protein counts between 31 and 54, genome lengths of 24.7 bp and 47.7 bp, and average GC content of 51.25%. In the phylogenetic analysis, the genomes of strains isolated from poultry in Brazil clustered into well-supported clades with a heterogeneous distribution, primarily associated with strains isolated from humans and food. The phylogenetic relationship of Brazilian S. Mbandaka suggests the presence of strains with high epidemiological significance and the potential to be linked to foodborne outbreaks. Overall, our results show that isolated strains of S. Mbandaka are multidrug-resistant and encode a rather conserved virulence machinery, which is an epidemiological hallmark of Salmonella strains that have successfully disseminated both regionally and globally.
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spelling Genomic Features and Phylogenetic Analysis of Antimicrobial-Resistant Salmonella Mbandaka ST413 StrainsSalmoneloseFatores de virulênciaBacteriófagosPatogêneseIn recent years, Salmonella enterica subsp. enterica serovar Mbandaka (S. Mbandaka) has been increasingly isolated from laying hens and shell eggs around the world. Moreover, this serovar has been identified as the causative agent of several salmonellosis outbreaks in humans. Surprisingly, little is known about the characteristics of this emerging serovar, and therefore, we investigated antimicrobial resistance, virulence, and prophage genes of six selected Brazilian strains of Salmonella Mbandaka using Whole Genome Sequencing (WGS). Multi-locus sequence typing revealed that the tested strains belong to Sequence Type 413 (ST413), which has been linked to recent multi-country salmonellosis outbreaks in Europe. A total of nine resistance genes were detected, and the most frequent ones were aac(6′)-Iaa, sul1, qacE, blaOXA-129, tet(B), and aadA1. A point mutation in ParC at the 57th position (threonine → serine) associated with quinolone resistance was present in all investigated genomes. A 112,960 bp IncHI2A plasmid was mapped in 4/6 strains. This plasmid harboured tetracycline (tetACDR) and mercury (mer) resistance genes, genes contributing to conjugative transfer, and genes involved in plasmid maintenance. Most strains (four/six) carried Salmonella genomic island 1 (SGI1). All S. Mbandaka genomes carried seven pathogenicity islands (SPIs) involved in intracellular survival and virulence: SPIs 1-5, 9, and C63PI. The virulence genes csgC, fimY, tcfA, sscA, (two/six), and ssaS (one/six) were absent in some of the genomes; conversely, fimA, prgH, and mgtC were present in all of them. Five Salmonella bacteriophage sequences (with homology to Escherichia phage phiV10, Enterobacteria phage Fels-2, Enterobacteria phage HK542, Enterobacteria phage ST64T, Salmonella phage SW9) were identified, with protein counts between 31 and 54, genome lengths of 24.7 bp and 47.7 bp, and average GC content of 51.25%. In the phylogenetic analysis, the genomes of strains isolated from poultry in Brazil clustered into well-supported clades with a heterogeneous distribution, primarily associated with strains isolated from humans and food. The phylogenetic relationship of Brazilian S. Mbandaka suggests the presence of strains with high epidemiological significance and the potential to be linked to foodborne outbreaks. Overall, our results show that isolated strains of S. Mbandaka are multidrug-resistant and encode a rather conserved virulence machinery, which is an epidemiological hallmark of Salmonella strains that have successfully disseminated both regionally and globally.Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)Versão final do editorFAPESP: 2020/07018-6FAPESP: 2021/10285-9CAPES: 001MDPI2024-03-04T13:09:27Z2024-03-04T13:09:27Z2024-02-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlePDF16 p.application/pdf2076-2607https://hdl.handle.net/11449/253509https://doi.org/10.3390/microorganisms12020312854959705710317968499351030783177207595002088908108581083285198935080962606782860000-0002-7552-16070000-0003-1875-44950000-0002-8639-40760000-0001-5380-80950000-0002-7761-06970000-0002-6333-52680000-0003-0574-98650000-0003-4238-46580000-0001-6225-65870000-0003-2522-6500enghttps://hdl.handle.net/11449/255888MicroorganismsBenevides, Valdinete PereiraSaraiva, Mauro de Mesquita SouzaNascimento, Camila de FátimaDelgado-Suárez, Enrique JesúsOliveira, Celso José BrunoSilva, Saura RodriguesMiranda, Vitor Fernandes OliveiraChristensen, HenrikOlsen, John ElmerdahlBerchieri Junior, Angeloinfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESP2024-06-12T12:47:16Zoai:repositorio.unesp.br:11449/253509Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T17:28:51.576912Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Genomic Features and Phylogenetic Analysis of Antimicrobial-Resistant Salmonella Mbandaka ST413 Strains
title Genomic Features and Phylogenetic Analysis of Antimicrobial-Resistant Salmonella Mbandaka ST413 Strains
spellingShingle Genomic Features and Phylogenetic Analysis of Antimicrobial-Resistant Salmonella Mbandaka ST413 Strains
Benevides, Valdinete Pereira
Salmonelose
Fatores de virulência
Bacteriófagos
Patogênese
title_short Genomic Features and Phylogenetic Analysis of Antimicrobial-Resistant Salmonella Mbandaka ST413 Strains
title_full Genomic Features and Phylogenetic Analysis of Antimicrobial-Resistant Salmonella Mbandaka ST413 Strains
title_fullStr Genomic Features and Phylogenetic Analysis of Antimicrobial-Resistant Salmonella Mbandaka ST413 Strains
title_full_unstemmed Genomic Features and Phylogenetic Analysis of Antimicrobial-Resistant Salmonella Mbandaka ST413 Strains
title_sort Genomic Features and Phylogenetic Analysis of Antimicrobial-Resistant Salmonella Mbandaka ST413 Strains
author Benevides, Valdinete Pereira
author_facet Benevides, Valdinete Pereira
Saraiva, Mauro de Mesquita Souza
Nascimento, Camila de Fátima
Delgado-Suárez, Enrique Jesús
Oliveira, Celso José Bruno
Silva, Saura Rodrigues
Miranda, Vitor Fernandes Oliveira
Christensen, Henrik
Olsen, John Elmerdahl
Berchieri Junior, Angelo
author_role author
author2 Saraiva, Mauro de Mesquita Souza
Nascimento, Camila de Fátima
Delgado-Suárez, Enrique Jesús
Oliveira, Celso José Bruno
Silva, Saura Rodrigues
Miranda, Vitor Fernandes Oliveira
Christensen, Henrik
Olsen, John Elmerdahl
Berchieri Junior, Angelo
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Benevides, Valdinete Pereira
Saraiva, Mauro de Mesquita Souza
Nascimento, Camila de Fátima
Delgado-Suárez, Enrique Jesús
Oliveira, Celso José Bruno
Silva, Saura Rodrigues
Miranda, Vitor Fernandes Oliveira
Christensen, Henrik
Olsen, John Elmerdahl
Berchieri Junior, Angelo
dc.subject.por.fl_str_mv Salmonelose
Fatores de virulência
Bacteriófagos
Patogênese
topic Salmonelose
Fatores de virulência
Bacteriófagos
Patogênese
description In recent years, Salmonella enterica subsp. enterica serovar Mbandaka (S. Mbandaka) has been increasingly isolated from laying hens and shell eggs around the world. Moreover, this serovar has been identified as the causative agent of several salmonellosis outbreaks in humans. Surprisingly, little is known about the characteristics of this emerging serovar, and therefore, we investigated antimicrobial resistance, virulence, and prophage genes of six selected Brazilian strains of Salmonella Mbandaka using Whole Genome Sequencing (WGS). Multi-locus sequence typing revealed that the tested strains belong to Sequence Type 413 (ST413), which has been linked to recent multi-country salmonellosis outbreaks in Europe. A total of nine resistance genes were detected, and the most frequent ones were aac(6′)-Iaa, sul1, qacE, blaOXA-129, tet(B), and aadA1. A point mutation in ParC at the 57th position (threonine → serine) associated with quinolone resistance was present in all investigated genomes. A 112,960 bp IncHI2A plasmid was mapped in 4/6 strains. This plasmid harboured tetracycline (tetACDR) and mercury (mer) resistance genes, genes contributing to conjugative transfer, and genes involved in plasmid maintenance. Most strains (four/six) carried Salmonella genomic island 1 (SGI1). All S. Mbandaka genomes carried seven pathogenicity islands (SPIs) involved in intracellular survival and virulence: SPIs 1-5, 9, and C63PI. The virulence genes csgC, fimY, tcfA, sscA, (two/six), and ssaS (one/six) were absent in some of the genomes; conversely, fimA, prgH, and mgtC were present in all of them. Five Salmonella bacteriophage sequences (with homology to Escherichia phage phiV10, Enterobacteria phage Fels-2, Enterobacteria phage HK542, Enterobacteria phage ST64T, Salmonella phage SW9) were identified, with protein counts between 31 and 54, genome lengths of 24.7 bp and 47.7 bp, and average GC content of 51.25%. In the phylogenetic analysis, the genomes of strains isolated from poultry in Brazil clustered into well-supported clades with a heterogeneous distribution, primarily associated with strains isolated from humans and food. The phylogenetic relationship of Brazilian S. Mbandaka suggests the presence of strains with high epidemiological significance and the potential to be linked to foodborne outbreaks. Overall, our results show that isolated strains of S. Mbandaka are multidrug-resistant and encode a rather conserved virulence machinery, which is an epidemiological hallmark of Salmonella strains that have successfully disseminated both regionally and globally.
publishDate 2024
dc.date.none.fl_str_mv 2024-03-04T13:09:27Z
2024-03-04T13:09:27Z
2024-02-01
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url https://hdl.handle.net/11449/253509
https://doi.org/10.3390/microorganisms12020312
dc.language.iso.fl_str_mv eng
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dc.relation.none.fl_str_mv https://hdl.handle.net/11449/255888
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