Staphylococcus argenteus isolated from retail foods in China: Incidence, antibiotic resistance, biofilm formation and toxin gene profile

Staphylococcus argenteus is a novel species of coagulase-positive staphylococci which was separated from Staphylococcus aureus in 2014. It can threaten human health like S. aureus but can not identify with conventional biochemical or other phenotypic testing. From 2011 to 2016, 1581 S. aureus strains were isolated from 4300 samples from retail foods covering most provincial capitals in China. According to multilocus sequence typing (MLST) and PCR confirmation, 7.2% of isolates (114/1581) were confirmed as S. argenteus. The pathogen was distributed in 22 of 39 sampled cities and all food types. Interestingly, most S. argenteus positive samples were collected from coastal cities in South China. MLST detected 8 different sequence types (STs), including five new STs. CC2250 was the predominant lineage of S. argenteus, followed by CC1223. To further characterize the isolates, their antibiotic resistance, virulence genes, biofilm formation and biofilm-related genes were examined. The pvl gene was not detected in S. argenteus, and only 1 isolate (0.9%) was positive for the tsst-1 gene. For 18 enterotoxin genes, 16.7% (19/114) of isolates harboured more than three genes, whereas 70.2% (80/114) of isolates had none of the investigated genes. Penicillin and ampicillin were the major antibiotics to which the S. argenteus isolates were resistant, followed by tetracycline, kanamycin and fusidic acid. A total of 94.7% of isolates had the ability to produce biofilms and all isolates harboured icaA, fnbA, and fib genes. Other biofilm-related genes, such as eno, clfB, fnbB, and icaC, were also found in 99.1%, 92.1%, 88.6%, and 74.6% of isolates, respectively. This study is the first systematic investigation of the prevalence of S. argenteus in retail foods in China and shows their ubiquity in food. We also provide comprehensive surveillance of the incidence of S. argenteus in retail foods and information to enable more accurate and effective treatment of infections of this new species.