AUTHOR=Liu Hui , Ji Xing , Wang Heye , Hou Xiang , Sun Haichang , Billington Craig , Zhang Lili , Wang Xiaoye , Wang Ran 

TITLE=Genomic epidemiology and characterization of Staphylococcus aureus isolates from raw milk in Jiangsu, China: emerging broader host tropism strain clones ST59 and ST398

JOURNAL=Frontiers in Microbiology

VOLUME=14

YEAR=2023

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2023.1266715

DOI=10.3389/fmicb.2023.1266715

ISSN=1664-302X

ABSTRACT=<p><italic>Staphylococcus aureus</italic> is highly pathogenic and can cause disease in both humans and domestic animals. The aim of this study was to investigate the genomic epidemiology of <italic>S. aureus</italic> isolates from raw milk in Jiangsu Province, China, to identify predominant lineages and their associated genomic and phenotypic characteristics. In this study, we identified 117 <italic>S. aureus</italic> isolates collected from 1,062 samples in Jiangsu Province between 2021 and 2022. Based on whole-genome sequencing (WGS) data from 117 <italic>S. aureus</italic> isolates, molecular analyses indicated CC1-ST1 (26.50%, 31/117), CC97-ST97 (18.80%, 22/117), CC398-ST398 (10.26%, 12/117), CC8-ST630 (7.69%, 9/117) and CC59-ST59 (2.56%, 3/117) were the major lineages. The prevalence of <italic>mecA</italic>-positive strains was 11.11%. Four methicillin-resistant <italic>S. aureus</italic> (MRSA) lineages were found, including MRSA-ST59-t172 (<italic>n</italic> = 3), OS-MRSA-ST398-t011 (<italic>n</italic> = 1), MRSA-ST630-t2196 (<italic>n</italic> = 2) and OS-MRSA-ST630-t2196 (<italic>n</italic> = 7). Phenotypic resistance to penicillin (30.77%, 36/117), ciprofloxacin (17.09%, 20/117) and erythromycin (15.38%, 18/117) was observed which corresponded with resistance genotypes. All of the isolates could produce biofilms, and 38.46% (45/117) of isolates had invasion rates in mammary epithelial cells (MAC-T) of greater than 1%. Interestingly, most biofilm-producing and invading isolates harbored <italic>ebp</italic>-<italic>icaA</italic>-<italic>icaB</italic>-<italic>icaC</italic>-<italic>icaR</italic>-<italic>clfA</italic>-<italic>clfB</italic>-<italic>fnbA</italic>-<italic>fnbB</italic>-<italic>sdrC</italic>-<italic>sdrD</italic>-<italic>sdrE</italic>-<italic>map</italic>-<italic>can</italic> (27.35%, 32/117) and <italic>ebp</italic>-<italic>icaA</italic>-<italic>icaB</italic>-<italic>icaC</italic>-<italic>icaD</italic>-<italic>icaR</italic>-<italic>clfA</italic>-<italic>clfB</italic>-<italic>fnbA</italic>-<italic>fnbB</italic>-<italic>sdrC</italic>-<italic>sdrD</italic>-<italic>sdrE</italic>-<italic>map</italic> (33.33%, 39/117) adherence-associated gene patterns and belonged to lineages CC1 and CC97, respectively. Virulence factor assays showed that 47.01% of the isolates contained at least enterotoxin genes. Isolates harboring the immune evasion cluster (IEC) genes (<italic>sea</italic>, <italic>sak</italic>, <italic>chp</italic>, and <italic>scn</italic>) were predominantly categorized as STs 464, 398, and 59. IEC-positive ST398 and ST59 isolates contained a very high proportion of virulence genes located on prophages, whereas most IEC-negative ST398 clade isolates carried broad-spectrum drug resistance genes. Meanwhile, the IEC-positive ST398 clade showed a close genetic relationship with isolates from the pork supply chain and hospital surgical site infections. MRSA-ST59 strains showed the closest genetic relationship with an isolate from quick-frozen products. High-risk livestock-associated strains ST398 and MRSA-ST59 were detected in raw milk, indicating a potential public health risk of <italic>S. aureus</italic> transmission between livestock and humans. Our study highlights the necessity for <italic>S. aureus</italic> surveillance in the dairy industry.</p>