Study of the genomic diversity of Salmonella Agona in France: a persistent serotype?
Résumé
Salmonella spp. is a ubiquitous bacterium and the second most frequent cause of bacterial foodborne diseases in Europe. In this context, The French Agency for Food, Environmental and Occupational Health & Safety (Anses) monitors in France the occurrence of Salmonella strains in animal, food, feed and environment via the French National Reference Laboratory (NRL) for Salmonella and the Salmonella network. The NRL focuses on active surveillance in the poultry production while the Salmonella network centralizes data of non-human Salmonella. Likewise, the Institut Pasteur (Paris) hosts the French National Reference Centre for E. coli, Shigella & Salmonella (NRC-ESS) and surveils Salmonella isolated from humans. In Europe and particularly in France, Salmonella enterica subsp. enterica serotype Agona (S. Agona) appears in the top 20 of the most frequently isolated serotypes in human and non-human isolates. In France, since 2004, this serotype is mostly isolated from chicken, turkey, milk and dairy products and it has been responsible for two human outbreaks (in 2005 and 2018) linked to the consumption of contaminated infant formula1.
In this study, we investigated the genomic diversity of S. Agona on a large panel of human and non-human strains collected in France since 2004 by the French NRL, the Salmonella network and the NRC-ESS. Phylogeny study was performed based on the core genome by both Single locus polymorphism (SNPs) and core-genome Multi-Locus Sequence Typing (cgMLST) analyses. Homologous recombination events were searched and a full accessory genome characterization was carried out to detect pathogenicity island, genetic elements and/or plasmids that may have an impact of the capacity of S. Agona to survive in a processing plant, to contaminate food products and to infect human. Finally, to have a global view of the diversity of this serotype, the genomes of 187 strains isolated worldwide were downloaded from Enterobase public databases and integrated to the French panel to carry out a cgMLST analysis.
The phylogenetic analysis of the French strains highlighted the clonal structure of the population and revealed that ST13 is the most prevalent sequence type (ST) in France. Some strains associated to the human outbreaks seem to be linked and isolated from the same processing plant. The characterization of the accessory genome allowed us to identify genetic elements encoding resistance factors and genes conferring resistance to heavy metals and biocides, which are widely used in food processing industry.
These results provide an overview of the diversity of S. Agona in France over the past two decades and allowed us to identify markers contributing to the persistence of this serotype in processing plant.