Molecular Surveillance of MRSA in Raw Milk Provides Insight into MRSA Cross Species Evolution

ABSTRACT Methicillin-resistant Staphylococcus aureus (MRSA) in foods has been associated with severe infections in humans and animals worldwide. In the present study, the molecular characteristics of livestock-associated MRSA (LA-MRSA) and human-associated MRSA (hMRSA) isolates obtained in China, as well as MRSA isolates obtained from raw milk in 2018, were investigated. In total, 343 (20.38%; 343/1,683) S. aureus isolates were obtained from 1,683 raw milk samples from 100 dairy farms in 11 provinces across China. Among these, 49 (2.91%; 49/1,683) were mecA-positive MRSA. All LA-MRSA isolates were resistant to penicillin and highly resistant to erythromycin, sulfisoxazole, and clindamycin. Bioinformatic analysis the 49 genomes of LA-MRSA and 71 previously published hMRSA genomes isolated from Chinese individuals in 2018 indicated that blaZ, erm, ant(6)-Ia, aph(3′)-III, tet(K), cat, and aph(2″)-Ia were more prevalent in MRSA from raw milk (P < 0.05) compared to hMRSA. Additionally, hMRSA isolates were more significantly associated with ST5 (P < 0.01) compared to LA-MRSA; in contrast, ST338 was more prevalent among LA-MRSA isolates (P < 0.01). Likewise, the SCCmec type II was only detected in hMRSA isolates, whereas SCCmec type V and IV were more prevalent among LA-MRSA (P < 0.01). Furthermore, core-genome phylogenetic analysis showed the endemic characteristics of LA-MRSA in local provinces, as well as the close evolutionary relationships between MRSA from cattle and humans. Finally, homology analysis of mecA and blaZ genetic contexts revealed a high possibility of horizontal transmission of MRSA resistance genes among raw milk-associated and hMRSA strains, which increases the risk for public health. IMPORTANCE Methicillin-resistant Staphylococcus aureus (MRSA) is considered a public health concern as it is resistant to multiple antibiotics, thus being in zoonotic transmission of antibiotic resistance genes. MRSA causes serious public health issues and leads to hard-to-treat infections in humans and animals; therefore, it was meaningful to determine the prevalence of MRSA in raw milk samples and investigate phenotype and genotype of antimicrobial resistance and molecular characteristics in livestock-associated MRSA (LA-MRSA) and human-associated MRSA (hMRSA) in China, which could provide a theoretical basis for preventing and controlling the spread of MRSA between livestock and humans.