Distinct Phenotypic and Genomic Signatures Underlie Contrasting Pathogenic Potential of Staphylococcus epidermidis Clonal Lineages
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...
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| Format: | Article |
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Frontiers Media S.A.
2019-08-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2019.01971/full |
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| author | Diana Espadinha Diana Espadinha Rita G. Sobral Catarina Inês Mendes Guillaume Méric Samuel K. Sheppard Samuel K. Sheppard João A. Carriço Hermínia de Lencastre Hermínia de Lencastre Maria Miragaia |
| author_facet | Diana Espadinha Diana Espadinha Rita G. Sobral Catarina Inês Mendes Guillaume Méric Samuel K. Sheppard Samuel K. Sheppard João A. Carriço Hermínia de Lencastre Hermínia de Lencastre Maria Miragaia |
| author_sort | Diana Espadinha |
| collection | DOAJ |
| description | 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. Staphylococcus 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 catalog of putative S. epidermidis virulence factors and identified an epidemiological molecular marker for the more pathogenic lineage.Conclusion: 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. |
| first_indexed | 2024-12-10T08:16:26Z |
| format | Article |
| id | doaj.art-e470b3830555402e9fca68b19ba33772 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-10T08:16:26Z |
| publishDate | 2019-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-e470b3830555402e9fca68b19ba337722022-12-22T01:56:27ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-08-011010.3389/fmicb.2019.01971463823Distinct Phenotypic and Genomic Signatures Underlie Contrasting Pathogenic Potential of Staphylococcus epidermidis Clonal LineagesDiana Espadinha0Diana Espadinha1Rita G. Sobral2Catarina Inês Mendes3Guillaume Méric4Samuel K. Sheppard5Samuel K. Sheppard6João A. Carriço7Hermínia de Lencastre8Hermínia de Lencastre9Maria Miragaia10Laboratory of Bacterial Evolution and Molecular Epidemiology, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Oeiras, PortugalLaboratory of Molecular Genetics, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Oeiras, PortugalLaboratory of Molecular Microbiology of Bacterial Pathogens, UCIBIO/REQUIMTE, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Costa de Caparica, PortugalMolecular Microbiology and Infection Unit, Instituto de Medicina Molecular, Faculdade de Medicina de Lisboa, Universidade de Lisboa, Lisbon, PortugalThe Milner Centre for Evolution, University of Bath, Bath, United KingdomThe Milner Centre for Evolution, University of Bath, Bath, United KingdomMRC CLIMB Consortium, Bath, United KingdomMolecular Microbiology and Infection Unit, Instituto de Medicina Molecular, Faculdade de Medicina de Lisboa, Universidade de Lisboa, Lisbon, PortugalLaboratory of Molecular Genetics, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Oeiras, PortugalLaboratory of Microbiology and Infectious Diseases, The Rockefeller University, New York, NY, United StatesLaboratory of Bacterial Evolution and Molecular Epidemiology, Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Oeiras, PortugalBackground: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. Staphylococcus 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 catalog of putative S. epidermidis virulence factors and identified an epidemiological molecular marker for the more pathogenic lineage.Conclusion: 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.https://www.frontiersin.org/article/10.3389/fmicb.2019.01971/fullS. epidermidispan genomeGWASclonal lineagespathogencommensal |
| spellingShingle | Diana Espadinha Diana Espadinha Rita G. Sobral Catarina Inês Mendes Guillaume Méric Samuel K. Sheppard Samuel K. Sheppard João A. Carriço Hermínia de Lencastre Hermínia de Lencastre Maria Miragaia Distinct Phenotypic and Genomic Signatures Underlie Contrasting Pathogenic Potential of Staphylococcus epidermidis Clonal Lineages Frontiers in Microbiology S. epidermidis pan genome GWAS clonal lineages pathogen commensal |
| title | Distinct Phenotypic and Genomic Signatures Underlie Contrasting Pathogenic Potential of Staphylococcus epidermidis Clonal Lineages |
| title_full | Distinct Phenotypic and Genomic Signatures Underlie Contrasting Pathogenic Potential of Staphylococcus epidermidis Clonal Lineages |
| title_fullStr | Distinct Phenotypic and Genomic Signatures Underlie Contrasting Pathogenic Potential of Staphylococcus epidermidis Clonal Lineages |
| title_full_unstemmed | Distinct Phenotypic and Genomic Signatures Underlie Contrasting Pathogenic Potential of Staphylococcus epidermidis Clonal Lineages |
| title_short | Distinct Phenotypic and Genomic Signatures Underlie Contrasting Pathogenic Potential of Staphylococcus epidermidis Clonal Lineages |
| title_sort | distinct phenotypic and genomic signatures underlie contrasting pathogenic potential of staphylococcus epidermidis clonal lineages |
| topic | S. epidermidis pan genome GWAS clonal lineages pathogen commensal |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2019.01971/full |
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