Salmonella Agona inside and outside the French borders: phylogenomic diversity, plasmidome, resistome and virulome.
This study reveals that the dominant lineage of Salmonella Agona is highly prevalent and genetically diverse, with significant implications for public health monitoring.
Where it sits
this study against the rest of the selank corpusSummary and findings
This study investigated the population structure and genetic determinants of Salmonella enterica serotype Agona (S. Agona) using 4202 genomes collected worldwide from 1952 to 2025. Whole-genome analyses revealed a dominant lineage (ST13) accounting for approximately 99% of genomes, with significant microdiversity observed. The research highlights complex transmission pathways and the presence of antimicrobial resistance genes.
Abstract
Salmonella enterica serotype Agona (S. Agona) is a globally distributed foodborne pathogen associated with diverse hosts, environments, and foodborne outbreaks. We investigated its population structure, global dissemination, and the genetic determinants underlying the ecological adaptation and epidemiological success of strains implicated in nationwide alerts in France in 2005 and 2017. A total of 4202 genomes from isolates collected worldwide between 1952 and 2025 were analyzed, including 141 newly sequenced genomes representative of agri-food sectors in France. Whole-genome analyses confirmed the polyphyletic nature of S. Agona, while cgMLST hierarchical clustering at the HC900 level identified two major genomic lineages differing in type VI secretion system (T6SS) patterns and the presence of Salmonella pathogenicity island 17 (SPI-17). The dominant lineage (ST13) accounted for approximately 99% of genomes and displayed broad distribution across hosts and ecological niches worldwide. Despite core genome conservation, fine-scale HC5 clustering revealed substantial microdiversity with 1771 clusters, including 229 identified among isolates from France, 183 of which were unique to the country. Phylogenetic analysis of 233 human and agri-food isolates from France suggested complex transmission pathways between environmental, food, and human reservoirs and demonstrated that the 2017 infant formula outbreak in France originated from direct descendants of the 2005 outbreak clone. Accessory genome analysis revealed genes associated with tolerance to metals, biocides, and antimicrobials, two independently acquired Salmonella genomic island-4-like elements, and 133 predicted plasmids, collectively encoding 26 carrying antimicrobial resistance genes. These findings provide new insights into the evolution, ecological versatility, and public health significance of S. Agona.
Background
The paper addresses the phylogenomic diversity and ecological adaptation of Salmonella enterica serotype Agona, a foodborne pathogen linked to outbreaks. Prior knowledge indicated that S. Agona is globally distributed, but detailed genomic insights were lacking. This study is significant as it provides a comprehensive analysis of the genetic factors contributing to the pathogen's epidemiological success.
Methods
The study utilized whole-genome sequencing to analyze 4202 genomes of S. Agona isolates. The population structure was assessed using cgMLST hierarchical clustering, focusing on the identification of genomic lineages and microdiversity. The analysis included 141 newly sequenced genomes from France's agri-food sectors.
Results
The primary finding was that the dominant lineage (ST13) accounted for approximately 99% of genomes. The study identified 1771 clusters, with 229 being unique to France. Phylogenetic analysis indicated complex transmission pathways, particularly linking the 2017 infant formula outbreak to the 2005 outbreak clone.
Interpretation
The findings align with previous literature on the global distribution of S. Agona but provide new insights into its genetic diversity and resistance mechanisms. While the statistical significance of the findings is clear, the clinical implications regarding public health require further investigation. Limitations include potential confounding factors such as the study's reliance on genomic data without direct clinical outcomes.
Key findings
- 4202 genomes analyzed from isolates collected worldwide between 1952 and 2025.
- Dominant lineage (ST13) accounted for approximately 99% of genomes.
- 1771 clusters identified, with 229 unique to France.
- 233 human and agri-food isolates from France analyzed.
- 26 antimicrobial resistance genes identified across 133 predicted plasmids.
Limitations
- Not reported in abstract.
- Study relies on genomic data without direct clinical outcomes.
- Potential confounding factors not addressed.