Comparative Genomic Analyses Reveal Potential Factors Responsible for the ST6 Oxacillin-Resistant Staphylococcus lugdunensis Endemic in a Hospital

Shih-Cheng Chang; Lee-Chung Lin; Jang-Jih Lu

doi:10.3389/fmicb.2021.765437

Comparative Genomic Analyses Reveal Potential Factors Responsible for the ST6 Oxacillin-Resistant Staphylococcus lugdunensis Endemic in a Hospital

Front Microbiol. 2021 Nov 25:12:765437. doi: 10.3389/fmicb.2021.765437. eCollection 2021.

Authors

Shih-Cheng Chang^{1

2}, Lee-Chung Lin¹, Jang-Jih Lu^{1

2

3}

Affiliations

¹ Department of Laboratory Medicine, Linkou Chang Gung Memorial Hospital, Taoyuan, Taiwan.
² Department of Medical Biotechnology and Laboratory Science, College of Medicine, Chang Gung University, Taoyuan, Taiwan.
³ Department of Medicine, College of Medicine, Chang Gung University, Taoyuan, Taiwan.

Abstract

Oxacillin-resistant Staphylococcus lugdunensis (ORSL) is considered a life-threatening isolate in healthcare settings. Among ORSL clones, ST6-SCCmec II strains are associated with an endemic spread in hospitals. We analyzed the complete genome of ORSL CGMH-SL118, a representative strain. Results revealed that this strain contained three MGEs (two prophages and one plasmid) other than the SCCmec II element, which showed remarkable differences in genome organization compared to the reference strains from NCBI. Eight multidrug-resistant genes were identified. All but blaZ were carried by MGEs, such as the SCCmec II element [mecA, ant (9)-Ia, and ermA] and the prophage φSPbeta [aac (6')-aph (2'), aph (3')-III, and ant (6)-Ia], indicating that MGEs carrying multidrug-resistant genes may be important for ST6 strains. The prophage φSPbeta contains sasX gene, which was responsible for the pathogenesis of Staphylococcus aureus. A phage-mediated resistant island containing fusB (SlRI _fusB-118) was found near φSPbeta, which was highly homologous to type III SeRI _fusB-5907 of Staphylococcus epidermidis. In contrast to previous studies, over 20% of ST6 isolates showed a fusidic acid-resistant phenotype, suggesting that phage-mediated intraspecies transmission of resistant islands may become an important issue for ST6 strains. Sixty-eight clinical isolates of ST6 Staphylococcus lugdunensis (50 OSSL, oxacillin-sensitive S. lugdunensis, and 18 ORSL, including CGMH-SL118) collected from various types of specimens in the hospital were studied. Among these isolates in this study, ORSL showed similar drug-resistant genes and phenotypes as CGMH-SL118. The comparative genomic analyses highlight the contribution of MGEs in the development and dissemination of antimicrobial resistance in ST6 strains, suggesting that resistance determinants and virulence factors encoded by MGEs provide a survival advantage for successful colonization and spread in healthcare settings.

Keywords: mobile genetic elements; multidrug-resistant genes; oxacillin-resistant Staphylococcus lugdunensis; prophage; resistant islands.