Phylogeographical structure and genetic introgression in Salmonella enterica serotype Napoli: a genomic epidemiology...

Salmonella enterica serotype Napoli (S Napoli), a non-typhoidal Salmonella serotype that has been emerging in Italy, Switzerland, and France since the mid-1990s, has an unusual epidemiological profile that suggests a role for the environment in the transmission of these bacteria. The genomics of S Napoli has been inadequately characterised; we, therefore, aimed to provide a robust genomic framework for S Napoli surveillance.

In this genomic epidemiology study, we performed short-read sequencing of 1145 S Napoli isolates from national surveillance in four European countries (Italy, Switzerland, France, and Spain) and complemented this dataset with 175 additional genomes (174 published and one unpublished). We used the EnteroBase core genome multilocus sequence typing (cgMLST) scheme and its associated Hierarchical Clustering algorithm, along with other genome-based bioinformatics approaches such as single nucleotide variant-based phylogenetic analyses, ResFinder, PlasmidFinder, and RefSeq genomes, to characterise population structure, antimicrobial resistance (AMR) prevalence, and differences in gene content among genetic lineages.

We analysed 1320 S Napoli genomes, collected between April, 1945, and September 14, 2022, from human (n=1088, 82·4%) and non-human (n=232, 17·6%) sources in Italy (n=317, 24%), Switzerland (n=181, 13·7%), France (n=773, 58·5%), and Spain (n=48, 3·6%), confirming that the rising prevalence of S Napoli is driven by a single monophyletic serotype within cgMLST superlineage HC2000_1289. However, this serotype displays considerable genetic diversity (15 lineages falling into 12 HC900 clusters), strong spatial structuring, and a low frequency (2%) of AMR determinants. We also detected genetic introgression between S Napoli and the sympatric, closely related Salmonella enterica serotype Veneziana.

Unlike successful non-typhoidal Salmonella serotypes, for which globalisation has had a homogenising effect, S Napoli forms distinct lineages isolated by geographical distance. This study suggests that the persistence of S Napoli as a geographically structured metapopulation, causing localised human infections, could reflect the natural ecology of Salmonella before the rise of agribusiness. Future research should investigate the environmental reservoirs and transmission pathways of S Napoli.

Fondation Le Roch-Les Mousquetaires, Institut Pasteur, Santé publique France, Investissement d'Avenir programme, Laboratoire d'Excellence 'Integrative Biology of Emerging Infectious Diseases', and Institute of Health Carlos III 'Acción Estratégica de Salud Intramural'.