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Comparative genomics of Staphylococcus epidermidis from prosthetic-joint infections and nares highlights genetic traits associated with antimicrobial resistance, not virulence.

ABSTRACT: There is increased awareness of the worldwide spread of specific epidemic multidrug-resistant (MDR) lineages of the human commensal Staphylococcus epidermidis. Here, using bioinformatic analyses accounting for population structure, we determined genomic traits (genes, SNPs and k-mers) that distinguish S. epidermidis causing prosthetic-joint infections (PJIs) from commensal isolates from nares, by analysing whole-genome sequencing data from S. epidermidis from PJIs prospectively collected over 10 years in Sweden, and contemporary S. epidermidis from the nares of patients scheduled for arthroplasty surgery. Previously suggested virulence determinants and the presence of genes and mutations linked to antimicrobial resistance (AMR) were also investigated. Publicly available S. epidermidis sequences were used for international extrapolation and validation of findings. Our data show that S. epidermidis causing PJIs differed from nasal isolates not by virulence but by traits associated with resistance to compounds used in prevention of PJIs: β-lactams, aminoglycosides and chlorhexidine. Almost a quarter of the PJI isolates did not belong to any of the previously described major nosocomial lineages, but the AMR-related traits were also over-represented in these isolates, as well as in international S. epidermidis isolates originating from PJIs. Genes previously associated with virulence in S. epidermidis were over-represented in individual lineages, but failed to reach statistical significance when adjusted for population structure. Our findings suggest that the current strategies for prevention of PJIs select for nosocomial MDR S. epidermidis lineages that have arisen from horizontal gene transfer of AMR-related traits into multiple genetic backgrounds.

SUBMITTER: Mansson E

PROVIDER: S-EPMC8208700 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundStaphylococcus epidermidis has emerged as an often encountered pathogen responsible for hospital-acquired infections. The aim of present study is to investigate the microbiological characteristic of S. epidermidis isolates isolated from sterile specimens and skin in a Chinese tertiary hospital.MethodsA total of 223 non-duplicate S. epidermidis were collected from various sterile specimens of inpatients among 10 years in Wenzhou, China. 106 S. epidermidis obtained from the skin (urethral orifices) of healthy volunteers. All isolates were tested for antimicrobial susceptibility. PCR was used to detect the virulence- and resistance-associated genes and 7 housekeeping genes to determine the sequence types (STs) of selected isolates.ResultsThe resistance rates to antimicrobials tested except linezolid and vancomycin and the prevalence of methicillin-resistant S. epidermidis (MRSE) of S. epidermidis clinical isolates were significantly higher than those among colonized isolates (P < 0.05). The positive rates of virulence-associated genes including aap, sesI, ACME-arcA, IS256, bhp, altE, aae and gehD for S. epidermidis clinical isolates were significantly higher than those for colonized isolate (P < 0.05). A total of 60 STs including 28 from clinical isolates and 32 from colonized isolates were identified by MLST. A novel, rarely encountered clone, ST466, was found to be the second prevalent clone among clinical isolates. The great majority of the S. epidermidis isolates tested (73.86%) belonged to clone complex 2 (CC2). Compared with ST2, ST130, ST20 and ST59 clones, ST466 clone had the highest resistance rate to tetracycline (50.00%), the second highest prevalence of ACME-arcA (65.00%), bhp (30.00%) and qacA/B (65.00%), very low prevalence of carriage of icaA (0.00%) and biofilm formation (0.00%), the lack of sesI and high prevalence of aap, altE and aae (> 90%), which was similar to the characteristics of ST59 clone with one locus difference from ST466. ST466 clone competence with Staphylococcus aureus was relatively stronger, relative to ST2, ST20, ST130 and ST59 clones.ConclusionTaken together, a high-level of genetic diversity was found between clinical and colonized S. epidermidis isolates. A novel ST466 clone with distinct and similar characteristics relative to other prevalent clones, emerging as a prevalent clone in China, should be of major concern.

Project description:Staphylococcus epidermidis is a leading opportunistic pathogen causing nosocomial infections that is notable for its ability to form a biofilm and for its high rates of antibiotic resistance. It serves as a reservoir of multiple antimicrobial resistance genes that spread among the staphylococcal population by horizontal gene transfer such as transduction. While phage-mediated transduction is well studied in Staphylococcus aureus, S. epidermidis transducing phages have not been described in detail yet. Here, we report the characteristics of four phages, 27, 48, 456, and 459, previously used for S. epidermidis phage typing, and the newly isolated phage E72, from a clinical S. epidermidis strain. The phages, classified in the family Siphoviridae and genus Phietavirus, exhibited an S. epidermidis-specific host range, and together they infected 49% of the 35 strains tested. A whole-genome comparison revealed evolutionary relatedness to transducing S. aureus phietaviruses. In accordance with this, all the tested phages were capable of transduction with high frequencies up to 10-4 among S. epidermidis strains from different clonal complexes. Plasmids with sizes from 4 to 19 kb encoding resistance to streptomycin, tetracycline, and chloramphenicol were transferred. We provide here the first evidence of a phage-inducible chromosomal island transfer in S. epidermidis Similarly to S. aureus pathogenicity islands, the transfer was accompanied by phage capsid remodeling; however, the interfering protein encoded by the island was distinct. Our findings underline the role of S. epidermidis temperate phages in the evolution of S. epidermidis strains by horizontal gene transfer, which can also be utilized for S. epidermidis genetic studies.IMPORTANCE Multidrug-resistant strains of S. epidermidis emerge in both nosocomial and livestock environments as the most important pathogens among coagulase-negative staphylococcal species. The study of transduction by phages is essential to understanding how virulence and antimicrobial resistance genes spread in originally commensal bacterial populations. In this work, we provide a detailed description of transducing S. epidermidis phages. The high transduction frequencies of antimicrobial resistance plasmids and the first evidence of chromosomal island transfer emphasize the decisive role of S. epidermidis phages in attaining a higher pathogenic potential of host strains. To date, such importance has been attributed only to S. aureus phages, not to those of coagulase-negative staphylococci. This study also proved that the described transducing bacteriophages represent valuable genetic modification tools in S. epidermidis strains where other methods for gene transfer fail.

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Comparative genomics of Staphylococcus epidermidis from prosthetic-joint infections and nares highlights genetic traits associated with antimicrobial resistance, not virulence.

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