Prophage Integrase Typing Is a Useful Indicator of Genomic Diversity in Salmonella enterica

Salmonella enterica is a bacterial species that is a major cause of illness in humans and food-producing animals. S. enterica exhibits considerable inter-serovar diversity, as evidenced by the large number of host adapted serovars that have been identified. The development of methods to assess genom...

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Main Authors: Anna Colavecchio, Yasmin D’Souza, Elizabeth Tompkins, Julie Jeukens, Luca Freschi, Jean-Guillaume Emond-Rheault, Irena Kukavica-Ibrulj, Brian Boyle, Sadjia Bekal, Sandeep Tamber, Roger C. Levesque, Lawrence D. Goodridge
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-07-01
Series:Frontiers in Microbiology
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Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.01283/full
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author Anna Colavecchio
Yasmin D’Souza
Elizabeth Tompkins
Julie Jeukens
Luca Freschi
Jean-Guillaume Emond-Rheault
Irena Kukavica-Ibrulj
Brian Boyle
Sadjia Bekal
Sandeep Tamber
Roger C. Levesque
Lawrence D. Goodridge
author_facet Anna Colavecchio
Yasmin D’Souza
Elizabeth Tompkins
Julie Jeukens
Luca Freschi
Jean-Guillaume Emond-Rheault
Irena Kukavica-Ibrulj
Brian Boyle
Sadjia Bekal
Sandeep Tamber
Roger C. Levesque
Lawrence D. Goodridge
author_sort Anna Colavecchio
collection DOAJ
description Salmonella enterica is a bacterial species that is a major cause of illness in humans and food-producing animals. S. enterica exhibits considerable inter-serovar diversity, as evidenced by the large number of host adapted serovars that have been identified. The development of methods to assess genome diversity in S. enterica will help to further define the limits of diversity in this foodborne pathogen. Thus, we evaluated a PCR assay, which targets prophage integrase genes, as a rapid method to investigate S. enterica genome diversity. To evaluate the PCR prophage integrase assay, 49 isolates of S. enterica were selected, including 19 clinical isolates from clonal serovars (Enteritidis and Heidelberg) that commonly cause human illness, and 30 isolates from food-associated Salmonella serovars that rarely cause human illness. The number of integrase genes identified by the PCR assay was compared to the number of integrase genes within intact prophages identified by whole genome sequencing and phage finding program PHASTER. The PCR assay identified a total of 147 prophage integrase genes within the 49 S. enterica genomes (79 integrase genes in the food-associated Salmonella isolates, 50 integrase genes in S. Enteritidis, and 18 integrase genes in S. Heidelberg). In comparison, whole genome sequencing and PHASTER identified a total of 75 prophage integrase genes within 102 intact prophages in the 49 S. enterica genomes (44 integrase genes in the food-associated Salmonella isolates, 21 integrase genes in S. Enteritidis, and 9 integrase genes in S. Heidelberg). Collectively, both the PCR assay and PHASTER identified the presence of a large diversity of prophage integrase genes in the food-associated isolates compared to the clinical isolates, thus indicating a high degree of diversity in the food-associated isolates, and confirming the clonal nature of S. Enteritidis and S. Heidelberg. Moreover, PHASTER revealed a diversity of 29 different types of prophages and 23 different integrase genes within the food-associated isolates, but only identified four different phages and integrase genes within clonal isolates of S. Enteritidis and S. Heidelberg. These results demonstrate the potential usefulness of PCR based detection of prophage integrase genes as a rapid indicator of genome diversity in S. enterica.
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spelling doaj.art-68fe45af1d234c9c96a11683f72a47922022-12-22T01:05:33ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-07-01810.3389/fmicb.2017.01283271002Prophage Integrase Typing Is a Useful Indicator of Genomic Diversity in Salmonella entericaAnna Colavecchio0Yasmin D’Souza1Elizabeth Tompkins2Julie Jeukens3Luca Freschi4Jean-Guillaume Emond-Rheault5Irena Kukavica-Ibrulj6Brian Boyle7Sadjia Bekal8Sandeep Tamber9Roger C. Levesque10Lawrence D. Goodridge11Food Safety and Quality Program, Department of Food Science and Agricultural Chemistry, McGill University, Sainte-Anne-de-BellevueQC, CanadaFood Safety and Quality Program, Department of Food Science and Agricultural Chemistry, McGill University, Sainte-Anne-de-BellevueQC, CanadaFood Safety and Quality Program, Department of Food Science and Agricultural Chemistry, McGill University, Sainte-Anne-de-BellevueQC, CanadaInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec CityQC, CanadaInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec CityQC, CanadaInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec CityQC, CanadaInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec CityQC, CanadaInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec CityQC, CanadaPathogènes entériques et Bioterrorisme, Laboratoire de santé publique du Québec, Sainte-Anne-de-BellevueQC, CanadaSalmonella Research Laboratory, Bureau of Microbial Hazards, Health Canada, OttawaON, CanadaInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec CityQC, CanadaFood Safety and Quality Program, Department of Food Science and Agricultural Chemistry, McGill University, Sainte-Anne-de-BellevueQC, CanadaSalmonella enterica is a bacterial species that is a major cause of illness in humans and food-producing animals. S. enterica exhibits considerable inter-serovar diversity, as evidenced by the large number of host adapted serovars that have been identified. The development of methods to assess genome diversity in S. enterica will help to further define the limits of diversity in this foodborne pathogen. Thus, we evaluated a PCR assay, which targets prophage integrase genes, as a rapid method to investigate S. enterica genome diversity. To evaluate the PCR prophage integrase assay, 49 isolates of S. enterica were selected, including 19 clinical isolates from clonal serovars (Enteritidis and Heidelberg) that commonly cause human illness, and 30 isolates from food-associated Salmonella serovars that rarely cause human illness. The number of integrase genes identified by the PCR assay was compared to the number of integrase genes within intact prophages identified by whole genome sequencing and phage finding program PHASTER. The PCR assay identified a total of 147 prophage integrase genes within the 49 S. enterica genomes (79 integrase genes in the food-associated Salmonella isolates, 50 integrase genes in S. Enteritidis, and 18 integrase genes in S. Heidelberg). In comparison, whole genome sequencing and PHASTER identified a total of 75 prophage integrase genes within 102 intact prophages in the 49 S. enterica genomes (44 integrase genes in the food-associated Salmonella isolates, 21 integrase genes in S. Enteritidis, and 9 integrase genes in S. Heidelberg). Collectively, both the PCR assay and PHASTER identified the presence of a large diversity of prophage integrase genes in the food-associated isolates compared to the clinical isolates, thus indicating a high degree of diversity in the food-associated isolates, and confirming the clonal nature of S. Enteritidis and S. Heidelberg. Moreover, PHASTER revealed a diversity of 29 different types of prophages and 23 different integrase genes within the food-associated isolates, but only identified four different phages and integrase genes within clonal isolates of S. Enteritidis and S. Heidelberg. These results demonstrate the potential usefulness of PCR based detection of prophage integrase genes as a rapid indicator of genome diversity in S. enterica.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01283/fullSalmonella entericafoodborne pathogengenome diversityprophage integrase gene analysissignature genes
spellingShingle Anna Colavecchio
Yasmin D’Souza
Elizabeth Tompkins
Julie Jeukens
Luca Freschi
Jean-Guillaume Emond-Rheault
Irena Kukavica-Ibrulj
Brian Boyle
Sadjia Bekal
Sandeep Tamber
Roger C. Levesque
Lawrence D. Goodridge
Prophage Integrase Typing Is a Useful Indicator of Genomic Diversity in Salmonella enterica
Frontiers in Microbiology
Salmonella enterica
foodborne pathogen
genome diversity
prophage integrase gene analysis
signature genes
title Prophage Integrase Typing Is a Useful Indicator of Genomic Diversity in Salmonella enterica
title_full Prophage Integrase Typing Is a Useful Indicator of Genomic Diversity in Salmonella enterica
title_fullStr Prophage Integrase Typing Is a Useful Indicator of Genomic Diversity in Salmonella enterica
title_full_unstemmed Prophage Integrase Typing Is a Useful Indicator of Genomic Diversity in Salmonella enterica
title_short Prophage Integrase Typing Is a Useful Indicator of Genomic Diversity in Salmonella enterica
title_sort prophage integrase typing is a useful indicator of genomic diversity in salmonella enterica
topic Salmonella enterica
foodborne pathogen
genome diversity
prophage integrase gene analysis
signature genes
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.01283/full
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