Genomic and phenotypic characterization of multidrug-resistant <i>Staphylococcus haemolyticus</i> isolated from burn patients in Chongqing, southwestern China

<i>Staphylococcus hemolyticus</i> is one of the frequently isolated nosocomial pathogens in immunocompromised patients; however, its genotypic and phenotypic characteristics in burn patients remain largely unknown. In this study, 146 <i>S</i>. <i>haemolyticus</i> strains were collected from the burn unit of a tertiary hospital in Chongqing, southwestern China. Whole genome sequencing was applied to determine the molecular characteristics of these <i>S. haemolyticus</i> isolates. Results showed that sequence type 1 (ST1; 26.7%, 39/146) was the most prevalent lineage, followed by clones ST42 (17.8%, 25/146), ST3 (15.8%, 23/146), ST25 (9.6%, 14/146), ST29 (4.8%, 7/146), and newly emerged ST152 (6.2%, 9/146). In terms of phenotypes, 90.4% (132/146) of the <i>S. haemolyticus</i> isolates were multidrug-resistant (MDR), and more than 90% strains exhibited resistance to penicillin, erythromycin, oxacillin, and levofloxacin. A total of 145 out of 146 <i>S</i>. <i>haemolyticus</i> isolates harbored at least 10 virulence factor genes. The tested strains with ST1, ST3, ST25, and ST42 presented similar hemolytic activities and biofilm formation capabilities. All detected ST152 isolates were MDR, corresponding to the number of their antimicrobial resistance genes being the largest among all tested STs. Moreover, ST152 isolates had increased hemolytic capacity and biofilm formation capability compared with their counterpart ST29 strains, the parent lineage of ST152 with a single locus variation. Overall, this study showed the genomic and phenotypic characteristics of 146 <i>S</i>. <i>haemolyticus</i> strains isolated in Chongqing and found the newly emerged ST152 MDR lineage with hypervirulence, which may call attention to the control of infections caused by MDR <i>S. haemolyticus</i> strains in hospitals.IMPORTANCE<i>Staphylococcus haemolyticus</i> is a common opportunistic pathogen with multidrug resistance in clinical infections. In this study, we analyzed the molecular epidemiological characteristics of 146 <i>S</i>. <i>haemolyticus</i> strains isolated from the burn patients of a tertiary hospital in Chongqing between 2017 and 2023. The results demonstrated that the phylogenetic evolution of <i>S. haemolyticus</i> strains was diverse and plastic. The majority of the isolates were multidrug-resistant (MDR). The virulence genes, resistance elements, and phenotypes, such as hemolysis and biofilm formation, were determined. A new lineage (ST152) that harbored the highest number of resistance genes was characterized to be 100% (9/9) MDR. The prevalence of ST152 <i>S. haemolyticus</i> strains suggests a new health threat in terms of control and treatment of coagulase-negative staphylococcal infections in Chongqing. This study provides information for clinical control of <i>S. haemolyticus</i> dissemination and infection in hospitals.