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Original Research ARTICLE Provisionally accepted The full-text will be published soon. Notify me

Front. Microbiol. | doi: 10.3389/fmicb.2019.01971

Distinct phenotypic and genomic signatures underlie contrasting pathogenic potential of Staphylococcus epidermidis clonal lineages

  • 1Laboratory of Bacterial Evolution and Molecular Epidemiology, Institute of Chemical and Biological Technology, New University of Lisbon, Portugal
  • 2Laboratory of Molecular Microbiology of Bacterial Pathogens, UCIBIO@REQUIMTE, Department of Life Sciences, Faculty of Sciences and Technology, New University of Lisbon, Portugal
  • 3Molecular Microbiology and Infection Unit, Institute of Molecular Medicine, Faculty of Medicine, University of Lisbon, Portugal
  • 4Milner Centre for Evolution, University of Bath, United Kingdom
  • 5MRC CLIMB Consortium, United Kingdom, Milner Centre for Evolution, University of Bath, United Kingdom
  • 6Laboratory of Molecular Genetics, Institute of Chemical and Biological Technology, New University of Lisbon, Portugal
  • 7Labiratory of Bacterial Evolution and Molecular Epiemiology, Institute of Chemical and Biological Technology, New University of Lisbon, Portugal

Background: Staphylococcus epidermidis is a common skin commensal that has emerged as a pathogen in hospitals, mainly related to medical devices-associated infections. Noteworthy, infection rates by S. epidermidis have the tendency to rise steeply in next decades together with medical devices use and immunocompromized population growth.
S. epidermidis population structure includes two major clonal lineages (A/C and B) that present contrasting pathogenic potentials. To address this distinction and explore the basis of increased pathogenicity of A/C lineage, we performed a detailed comparative analysis using phylogenetic and integrated pangenome-wide-association study (panGWAS) approaches and compared the lineages’s phenotypes in in vitro conditions mimicking carriage and infection.
Results: Each S. epidermidis lineage had distinct phenotypic signatures in skin and infection conditions and differed in genomic content. Combination of phenotypic and genotypic data revealed that both lineages were well adapted to skin environmental cues. However, they appear to occupy different skin niches, perform distinct biological functions in the skin and use different mechanisms to complete the same function: lineage B strains showed evidence of specialization to survival in microaerobic and lipid rich environment, characteristic of hair follicle and sebaceous glands; lineage A/C strains showed evidence for adaption to diverse osmotic and pH conditions, potentially allowing them to occupy a broader and more superficial skin niche. In infection conditions, A/C strains had an advantage, having the potential to bind blood-associated host matrix proteins, form biofilms at blood pH, resist antibiotics and macrophage acidity and to produce proteases. These features were observed to be rare in the lineage B strains. PanGWAS analysis produced a catalogue of putative S. epidermidis virulence factors and identified an epidemiological molecular marker for the more pathogenic lineage.
Conclusions: The prevalence of A/C lineage in infection is probably related to a higher metabolic and genomic versatility that allows rapid adaptation during transition from a commensal to a pathogenic lifestyle. The putative virulence and phenotypic factors associated to A/C lineage constitute a reliable framework for future studies on S. epidermidis pathogenesis and the finding of an epidemiological marker for the more pathogenic lineage is an asset for the management of S. epidermidis infections

Keywords: Staphylococcus epidermidis, pangenome, GWAS, Clonal lineage, pathogen, commensal

Received: 02 Apr 2019; Accepted: 12 Aug 2019.

Copyright: © 2019 Espadinha, Sobral, Mendes, Meric, Sheppard, Carriço, De Lencastre and Miragaia. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Maria Miragaia, Institute of Chemical and Biological Technology, New University of Lisbon, Labiratory of Bacterial Evolution and Molecular Epiemiology, Oeiras, Portugal, miragaia@itqb.unl.pt