Prophage transduction promotes the transmission of phage resistance interfering with adsorption among Chinese foodborne Staphylococcus aureus

Although bacteriophages have proven to be efficient biocontrol agents for foodborne Staphylococcus aureus, the transmission of phage resistance resulting in the reduced efficacy of phage therapy remains to be explored. In this study, phage resistance and adsorption of 91 Chinese foodborne S. aureus isolates by 18 phages were estimated, and the distribution and transmission of phage resistance genes were investigated. The isolated 91 S. aureus comprised 50 multidrug-resistance isolates, all of which showed sensitivity to more than two phages. However, 9.9 % (9/91) of S. aureus isolates were resistant to all 18 phages, and the majority of phages (83.3 %, 15/18) did not adsorb to all foodborne S. aureus strains. Whole-genome analysis revealed that the 91 isolates comprised 101 phage resistance genes, including 24 genes were found in prophages (intact prophages, 19.8 %, 20/101; incomplete prophages, 16.8 %, 17/101). Notably, a temperate phage SapYZUs631 was successfully induced and exhibited better biological characteristics compared to other isolated S. aureus temperate phages, including higher titre (6.2 × 10⁹ PFU/mL), stronger pH (4–11) and thermal (60 °C for 60 min) stability, and a wider host range (80.2 %, 73/91). The SapYZUs631 genome contained phage resistance gene tarP interfering with adsorption and virulence genes. The lysogeny of SapYZUs631 into S. aureus strains YZUstau27, YZUstau31, and YZUstau35 resulted in increased phage resistance and decreased adsorption. Therefore, our analysis suggests that the interruption of adsorption is the main reason for the phage resistance of foodborne S. aureus in China, which resulted from the transmission of phage resistance by prophage transduction.