Monitoring longitudinal antimicrobial resistance trends of Staphylococcus aureus strains worldwide over the past 100 years to decipher its evolution and transmission

Staphylococcus aureus inhabits diverse habitats including food waste and wastewater treatment plants. Cases of S. aureus-induced infection are commonly reported worldwide. The emergence of antimicrobial resistance (AMR) of S. aureus is a growing public health threat worldwide. Here, we longitudinally monitored global trends in antibiotic resistance genes (ARGs) of 586 S. aureus strains, isolated between 1884 and 2022. The ARGs in S. aureus exhibited a significant increase over time (P < 0.0001). Mobile genetic elements play a crucial role in the transfer of ARGs in S. aureus strains. The structural equation model results revealed a significant correlation between the human development index and rising antibiotic consumption, which subsequently leads to an indirect escalation of AMR in S. aureus strains. Lastly, a machine learning algorithm successfully predicted the AMR risk of global terrestrial S. aureus with over 70% accuracy. Overall, these findings provided valuable insights for managing AMR in S. aureus. Staphylococcus aureus exhibits vital adaptability across diverse habitats including food waste and wastewater treatment plants. Cases of S. aureus-induced infection are frequently reported worldwide. The emergence of antimicrobial resistance (AMR) of S. aureus is a growing public health threat worldwide. Antibiotic resistance is the quintessential One Health and Global Health issue. Here, we longitudinally monitored global antibiotic resistance genes (ARGs) trends of S. aureus and found a distinct increase in AMR among S. aureus during recent decades. Besides, the driving factors of AMR are detected. These findings provided valuable insights for managing the AMR of S. aureus in waste treatment.