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Large-Scale Genomic Analyses and Toxinotyping of Clostridium perfringens Implicated in Foodborne Outbreaks in France

Clostridium perfringens is both an ubiquitous environmental bacterium and the fourth most common causative agent of foodborne outbreaks (FBOs) in France and Europe. These outbreaks are known to be caused by C. perfringens enterotoxin (CPE) encoded by the cpe gene. However, additional information on...

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Autores principales: Mahamat Abdelrahim, Abakabir, Radomski, Nicolas, Delannoy, Sabine, Djellal, Sofia, Le Négrate, Marylène, Hadjab, Katia, Fach, Patrick, Hennekinne, Jacques-Antoine, Mistou, Michel-Yves, Firmesse, Olivier
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6481350/
https://www.ncbi.nlm.nih.gov/pubmed/31057505
http://dx.doi.org/10.3389/fmicb.2019.00777
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author Mahamat Abdelrahim, Abakabir
Radomski, Nicolas
Delannoy, Sabine
Djellal, Sofia
Le Négrate, Marylène
Hadjab, Katia
Fach, Patrick
Hennekinne, Jacques-Antoine
Mistou, Michel-Yves
Firmesse, Olivier
author_facet Mahamat Abdelrahim, Abakabir
Radomski, Nicolas
Delannoy, Sabine
Djellal, Sofia
Le Négrate, Marylène
Hadjab, Katia
Fach, Patrick
Hennekinne, Jacques-Antoine
Mistou, Michel-Yves
Firmesse, Olivier
author_sort Mahamat Abdelrahim, Abakabir
collection PubMed
description Clostridium perfringens is both an ubiquitous environmental bacterium and the fourth most common causative agent of foodborne outbreaks (FBOs) in France and Europe. These outbreaks are known to be caused by C. perfringens enterotoxin (CPE) encoded by the cpe gene. However, additional information on the toxin/virulence gene content of C. perfringens has become available in the last few years. Therefore, to understand the enteropathogenicity of this bacterium, we need to describe the toxin and virulence genes content of strains involved in FBOs. In this study, we used a new real-time PCR typing technique based on a comprehensive set of 17 genes encoding virulence factors. The analysis was performed on a collection of 141 strains involved in 42 FBOs in the Paris region. It was combined with whole genome sequence (WGS) phylogenomic reconstruction, based on the coregenome single nucleotide polymorphisms (SNPs) of 58 isolates, representatives of the identified virulence gene profiles. Two or three different virulence gene profiles were detected in 10 FBOs, demonstrating that C. perfringens FBOs may be associated with heterogeneous strains. cpe-positive strains were isolated in 23 outbreaks, confirming the prominent role of CPE in pathogenicity. However, while C. perfringens was the sole pathogen isolated from the incriminated food, the cpe gene was not detected in strains related to 13 outbreaks. This result indicates either that the standard method was not able to isolate cpe+ strains or that the cpe gene may not be the only determinant of the enterotoxigenic potential of C. perfringens strains. Using phylogenomic reconstruction, we identified two clades distinguishing chromosomal cpe-positive from cpe-negative and plasmid-borne cpe. Important epidemiological information was also garnered from this phylogenomic reconstruction that revealed unexpected links between different outbreaks associated with closely related strains (seven SNP differences) and having common virulence gene profiles. This study provides new insight into the characterization of foodborne C. perfringens and highlights the potential of WGS for the investigation of FBOs.
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spelling pubmed-64813502019-05-03 Large-Scale Genomic Analyses and Toxinotyping of Clostridium perfringens Implicated in Foodborne Outbreaks in France Mahamat Abdelrahim, Abakabir Radomski, Nicolas Delannoy, Sabine Djellal, Sofia Le Négrate, Marylène Hadjab, Katia Fach, Patrick Hennekinne, Jacques-Antoine Mistou, Michel-Yves Firmesse, Olivier Front Microbiol Microbiology Clostridium perfringens is both an ubiquitous environmental bacterium and the fourth most common causative agent of foodborne outbreaks (FBOs) in France and Europe. These outbreaks are known to be caused by C. perfringens enterotoxin (CPE) encoded by the cpe gene. However, additional information on the toxin/virulence gene content of C. perfringens has become available in the last few years. Therefore, to understand the enteropathogenicity of this bacterium, we need to describe the toxin and virulence genes content of strains involved in FBOs. In this study, we used a new real-time PCR typing technique based on a comprehensive set of 17 genes encoding virulence factors. The analysis was performed on a collection of 141 strains involved in 42 FBOs in the Paris region. It was combined with whole genome sequence (WGS) phylogenomic reconstruction, based on the coregenome single nucleotide polymorphisms (SNPs) of 58 isolates, representatives of the identified virulence gene profiles. Two or three different virulence gene profiles were detected in 10 FBOs, demonstrating that C. perfringens FBOs may be associated with heterogeneous strains. cpe-positive strains were isolated in 23 outbreaks, confirming the prominent role of CPE in pathogenicity. However, while C. perfringens was the sole pathogen isolated from the incriminated food, the cpe gene was not detected in strains related to 13 outbreaks. This result indicates either that the standard method was not able to isolate cpe+ strains or that the cpe gene may not be the only determinant of the enterotoxigenic potential of C. perfringens strains. Using phylogenomic reconstruction, we identified two clades distinguishing chromosomal cpe-positive from cpe-negative and plasmid-borne cpe. Important epidemiological information was also garnered from this phylogenomic reconstruction that revealed unexpected links between different outbreaks associated with closely related strains (seven SNP differences) and having common virulence gene profiles. This study provides new insight into the characterization of foodborne C. perfringens and highlights the potential of WGS for the investigation of FBOs. Frontiers Media S.A. 2019-04-17 /pmc/articles/PMC6481350/ /pubmed/31057505 http://dx.doi.org/10.3389/fmicb.2019.00777 Text en Copyright © 2019 Mahamat Abdelrahim, Radomski, Delannoy, Djellal, Le Négrate, Hadjab, Fach, Hennekinne, Mistou and Firmesse. 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
Mahamat Abdelrahim, Abakabir
Radomski, Nicolas
Delannoy, Sabine
Djellal, Sofia
Le Négrate, Marylène
Hadjab, Katia
Fach, Patrick
Hennekinne, Jacques-Antoine
Mistou, Michel-Yves
Firmesse, Olivier
Large-Scale Genomic Analyses and Toxinotyping of Clostridium perfringens Implicated in Foodborne Outbreaks in France
title Large-Scale Genomic Analyses and Toxinotyping of Clostridium perfringens Implicated in Foodborne Outbreaks in France
title_full Large-Scale Genomic Analyses and Toxinotyping of Clostridium perfringens Implicated in Foodborne Outbreaks in France
title_fullStr Large-Scale Genomic Analyses and Toxinotyping of Clostridium perfringens Implicated in Foodborne Outbreaks in France
title_full_unstemmed Large-Scale Genomic Analyses and Toxinotyping of Clostridium perfringens Implicated in Foodborne Outbreaks in France
title_short Large-Scale Genomic Analyses and Toxinotyping of Clostridium perfringens Implicated in Foodborne Outbreaks in France
title_sort large-scale genomic analyses and toxinotyping of clostridium perfringens implicated in foodborne outbreaks in france
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6481350/
https://www.ncbi.nlm.nih.gov/pubmed/31057505
http://dx.doi.org/10.3389/fmicb.2019.00777
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