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Staphylococcus aureus  is a worldwide leading cause of numerous diseases ranging from food-poisoning to lethal infections. Methicillin-resistant  S. aureus  (MRSA) has been found capable of acquiring resistance to most antimicrobials. MRSA is ubiquitous and diverse even in terms of antimicrobial resistance (AMR) profiles, posing a challenge for treatment. Here, we present a comprehensive study of  S. aureus  in China, addressing epidemiology, phylogenetic reconstruction, genomic characterization, and identification of AMR profiles. The study analyzes 673  S. aureus  isolates from food as well as from hospitalized and healthy individuals. The isolates have been collected over a 9-year period, between 2010 and 2018, from 27 provinces across China. By whole-genome sequencing, Bayesian divergence analysis, and supervised machine learning, we reconstructed the phylogeny of the isolates and compared them to references from other countries. We identified 72 sequence types (STs), of which, 29 were novel. We found 81 MRSA lineages by multilocus sequence type (MLST),  spa , staphylococcal cassette chromosome  mec  element (SCC mec ), and Panton-Valentine leukocidin (PVL) typing. In addition, novel variants of SCC mec  type IV hosting extra metal and antimicrobial resistance genes, as well as a new SCC mec  type, were found. New Bayesian dating of the split times of major clades showed that ST9, ST59, and ST239 in China and European countries fell in different branches, whereas this pattern was not observed for the ST398 clone. On the contrary, the clonal transmission of ST398 was more intermixed in regard to geographic origin. Finally, we identified genetic determinants of resistance to 10 antimicrobials, discriminating drug-resistant bacteria from susceptible strains in the cohort. Our results reveal the emergence of Chinese MRSA lineages enriched of AMR determinants that share similar genetic traits of antimicrobial resistance across human and food, hinting at a complex scenario of evolving transmission routes.   IMPORTANCE  Little information is available on the epidemiology and characterization of  Staphylococcus aureus  in China. The role of food is a cause of major concern: staphylococcal foodborne diseases affect thousands every year, and the presence of resistant  Staphylococcus  strains on raw retail meat products is well documented. We studied a large heterogeneous data set of  S. aureus  isolates from many provinces of China, isolated from food as well as from individuals. Our large whole-genome collection represents a unique catalogue that can be easily meta-analyzed and integrated with further studies and adds to the library of  S. aureus  sequences in the public domain in a currently underrepresented geographical region. The new Bayesian dating of the split times of major drug-resistant enriched clones is relevant in showing that Chinese and European methicillin-resistant  S. aureus  (MRSA) have evolved differently. Our machine learning approach, across a large number of antibiotics, shows novel determinants underlying resistance and reveals frequent resistant traits in specific clonal complexes, highlighting the importance of particular clonal complexes in China. Our findings substantially expand what is known of the evolution and genetic determinants of resistance in food-associated  S. aureus  in China and add crucial information for whole-genome sequencing (WGS)-based surveillance of  S. aureus .

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Whole-Genome Sequencing and Machine Learning Analysis of Staphylococcus aureus from Multiple Heterogeneous Sources in China Reveals Common Genetic Traits of Antimicrobial Resistance