First report of enterotoxigenic Staphylococcus argenteus as a foodborne pathogen

Staphylococcal enterotoxins preformed in food are the causative agents of staphylococcal food poisoning outbreaks (SFPO). In this study we characterised in depth two coagulase-positive non-pigmented staphylococci involved in two independent outbreaks that occurred in France. While indistinguishable from Staphylococcus aureus using PCR methods and growth phenotype comparisons, both isolates were identified as Staphylococcus argenteus by whole genome sequencing. The genomes were analysed for the presence of enterotoxin genes, whose expression was determined in laboratory medium and, for the first time, in artificially-contaminated milk samples by using liquid chromatography-mass spectrometry and ELISA methods. The concentration measured for the SEB toxin in milk (0.67 ng/ml) was comparable to concentrations reported for other types of enterotoxins behind SFPO. From a collection of publicly available genomes, we performed an unprecedented systematic investigation of the enterotoxin gene set of S. argenteus, including variants and pseudogenes. The most prevalent genes were sex, followed by sel26, sel27 and sey. The egc cluster was less frequent and most of the time carried a dysfunctional seg gene. Our results shed light on the enterotoxigenic properties of S. argenteus, and emphasize the importance in monitoring of S. argenteus as an emerging foodborne pathogen.