Tell me if you prefer bovine or poultry sectors and I’ll tell you who you are: Characterization of Salmonella enterica subsp. enterica serovar Mbandaka in France

IntroductionIn north-western France, Salmonella enterica susp. enterica serovar Mbandaka (S. Mbandaka) is most frequently isolated from bovine and dairy samples. While this serovar most often results in asymptomatic carriage, for a number of years it has caused episodes of abortions, which have seri...

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Main Authors: Madeleine De Sousa Violante, Valérie Michel, Karol Romero, Laetitia Bonifait, Louise Baugé, Agnès Perrin-Guyomard, Carole Feurer, Nicolas Radomski, Ludovic Mallet, Michel-Yves Mistou, Sabrina Cadel-Six
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1130891/full
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author Madeleine De Sousa Violante
Madeleine De Sousa Violante
Valérie Michel
Karol Romero
Laetitia Bonifait
Louise Baugé
Agnès Perrin-Guyomard
Carole Feurer
Nicolas Radomski
Ludovic Mallet
Michel-Yves Mistou
Sabrina Cadel-Six
author_facet Madeleine De Sousa Violante
Madeleine De Sousa Violante
Valérie Michel
Karol Romero
Laetitia Bonifait
Louise Baugé
Agnès Perrin-Guyomard
Carole Feurer
Nicolas Radomski
Ludovic Mallet
Michel-Yves Mistou
Sabrina Cadel-Six
author_sort Madeleine De Sousa Violante
collection DOAJ
description IntroductionIn north-western France, Salmonella enterica susp. enterica serovar Mbandaka (S. Mbandaka) is most frequently isolated from bovine and dairy samples. While this serovar most often results in asymptomatic carriage, for a number of years it has caused episodes of abortions, which have serious economic consequences for the sector. Interestingly, this serovar is also isolated from Gallus gallus in the same geographic zone. Despite its prevalence in bovines in north-western France, S. Mbandaka has not been broadly studied at the genomic level, and its prevalence and host adaptation are still not fully understood.MethodsIn this study, we analyzed the genomic diversity of 304 strains of S. Mbandaka isolated from the bovine and poultry sectors in this area over a period of 5 years. A phylogenetic analysis was carried out and two approaches were followed to identify conserved genes and mutations related to host associations. The first approach targeted the genes compiled in the MEGARESv2, Resfinder, VFDB and SPI databases. Plasmid and phage contents were also investigated. The second approach refers to an in-house algorithm developed for this study that computes sensitivity, specificity, and accuracy of accessory genes and core variants according to predefined genomes groups.Results and discussionAll the analyzed strains belong to the multi-locus sequence type profile ST413, and the phylogenomic analysis revealed main clustering by host (bovine and poultry), emphasizing the circulation of 12 different major clones, of which seven circulate in poultry and five in the bovine sector in France and a likely food production chain adaptation of these clones. All strains present resistance determinants including heavy metals and biocides that could explain the ability of this serovar to survive and persist in the environment, within herds, and in food processing plants. To explore the wild animal contribution to the spread of this serovar in north-western France, we retrieved S. Mbandaka genomes isolated from wild birds from EnteroBase and included them in the phylogenomic analysis together with our collection. Lastly, screening of accessory genes and major variants allowed us to identify conserved specific mutations characteristic of each major cluster. These mutations could be used to design useful probes for food safety surveillance.
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spelling doaj.art-64ea3c6429ee4dcba2665ee8fadeedf92023-04-06T06:13:41ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-04-011410.3389/fmicb.2023.11308911130891Tell me if you prefer bovine or poultry sectors and I’ll tell you who you are: Characterization of Salmonella enterica subsp. enterica serovar Mbandaka in FranceMadeleine De Sousa Violante0Madeleine De Sousa Violante1Valérie Michel2Karol Romero3Laetitia Bonifait4Louise Baugé5Agnès Perrin-Guyomard6Carole Feurer7Nicolas Radomski8Ludovic Mallet9Michel-Yves Mistou10Sabrina Cadel-Six11INRAE, MaIAGE, Université Paris-Saclay, Jouy-en-Josas, FranceACTALIA, La Roche-sur-Foron, FranceACTALIA, La Roche-sur-Foron, FranceSalmonella and Listeria Unit (SEL), ANSES, Laboratory for Food Safety, Maisons-Alfort, FranceHygiene and Quality of Poultry and Pork Products Unit, ANSES, Ploufragan-Plouzané-Niort Laboratory, Ploufragan, FranceHygiene and Quality of Poultry and Pork Products Unit, ANSES, Ploufragan-Plouzané-Niort Laboratory, Ploufragan, FranceANSES, Fougères Laboratory, National Reference Laboratory for Antimicrobial Resistance, Fougères, FranceIFIP–Institut du Porc, Le Rheu, FranceIstituto Zooprofilattico Sperimentale dell’Abruzzo e del Molise “Giuseppe Caporale” (IZSAM), National Reference Centre (NRC) for Whole Genome Sequencing of Microbial Pathogens: Data-Base and Bioinformatics Analysis (GENPAT), Teramo, ItalyInstitut Universitaire du Cancer de Toulouse–Oncopole, Toulouse, FranceINRAE, MaIAGE, Université Paris-Saclay, Jouy-en-Josas, FranceSalmonella and Listeria Unit (SEL), ANSES, Laboratory for Food Safety, Maisons-Alfort, FranceIntroductionIn north-western France, Salmonella enterica susp. enterica serovar Mbandaka (S. Mbandaka) is most frequently isolated from bovine and dairy samples. While this serovar most often results in asymptomatic carriage, for a number of years it has caused episodes of abortions, which have serious economic consequences for the sector. Interestingly, this serovar is also isolated from Gallus gallus in the same geographic zone. Despite its prevalence in bovines in north-western France, S. Mbandaka has not been broadly studied at the genomic level, and its prevalence and host adaptation are still not fully understood.MethodsIn this study, we analyzed the genomic diversity of 304 strains of S. Mbandaka isolated from the bovine and poultry sectors in this area over a period of 5 years. A phylogenetic analysis was carried out and two approaches were followed to identify conserved genes and mutations related to host associations. The first approach targeted the genes compiled in the MEGARESv2, Resfinder, VFDB and SPI databases. Plasmid and phage contents were also investigated. The second approach refers to an in-house algorithm developed for this study that computes sensitivity, specificity, and accuracy of accessory genes and core variants according to predefined genomes groups.Results and discussionAll the analyzed strains belong to the multi-locus sequence type profile ST413, and the phylogenomic analysis revealed main clustering by host (bovine and poultry), emphasizing the circulation of 12 different major clones, of which seven circulate in poultry and five in the bovine sector in France and a likely food production chain adaptation of these clones. All strains present resistance determinants including heavy metals and biocides that could explain the ability of this serovar to survive and persist in the environment, within herds, and in food processing plants. To explore the wild animal contribution to the spread of this serovar in north-western France, we retrieved S. Mbandaka genomes isolated from wild birds from EnteroBase and included them in the phylogenomic analysis together with our collection. Lastly, screening of accessory genes and major variants allowed us to identify conserved specific mutations characteristic of each major cluster. These mutations could be used to design useful probes for food safety surveillance.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1130891/fullS. Mbandakabovine and poultry sectorsgenomic analysisclone characterizationgenomic markershost adaptation
spellingShingle Madeleine De Sousa Violante
Madeleine De Sousa Violante
Valérie Michel
Karol Romero
Laetitia Bonifait
Louise Baugé
Agnès Perrin-Guyomard
Carole Feurer
Nicolas Radomski
Ludovic Mallet
Michel-Yves Mistou
Sabrina Cadel-Six
Tell me if you prefer bovine or poultry sectors and I’ll tell you who you are: Characterization of Salmonella enterica subsp. enterica serovar Mbandaka in France
Frontiers in Microbiology
S. Mbandaka
bovine and poultry sectors
genomic analysis
clone characterization
genomic markers
host adaptation
title Tell me if you prefer bovine or poultry sectors and I’ll tell you who you are: Characterization of Salmonella enterica subsp. enterica serovar Mbandaka in France
title_full Tell me if you prefer bovine or poultry sectors and I’ll tell you who you are: Characterization of Salmonella enterica subsp. enterica serovar Mbandaka in France
title_fullStr Tell me if you prefer bovine or poultry sectors and I’ll tell you who you are: Characterization of Salmonella enterica subsp. enterica serovar Mbandaka in France
title_full_unstemmed Tell me if you prefer bovine or poultry sectors and I’ll tell you who you are: Characterization of Salmonella enterica subsp. enterica serovar Mbandaka in France
title_short Tell me if you prefer bovine or poultry sectors and I’ll tell you who you are: Characterization of Salmonella enterica subsp. enterica serovar Mbandaka in France
title_sort tell me if you prefer bovine or poultry sectors and i ll tell you who you are characterization of salmonella enterica subsp enterica serovar mbandaka in france
topic S. Mbandaka
bovine and poultry sectors
genomic analysis
clone characterization
genomic markers
host adaptation
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1130891/full
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