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Atopic dermatitis-derived Staphylococcus aureus strains: what makes them special in the interplay with the host

BACKGROUND: Atopic dermatitis (AD) is a chronic inflammatory skin condition whose pathogenesis involves genetic predisposition, epidermal barrier dysfunction, alterations in the immune responses and microbial dysbiosis. Clinical studies have shown a link between Staphylococcus aureus and the pathoge...

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Autores principales: Conte, Antonietta Lucia, Brunetti, Francesca, Marazzato, Massimiliano, Longhi, Catia, Maurizi, Linda, Raponi, Giammarco, Palamara, Anna Teresa, Grassi, Sara, Conte, Maria Pia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10303148/
https://www.ncbi.nlm.nih.gov/pubmed/37389215
http://dx.doi.org/10.3389/fcimb.2023.1194254
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author Conte, Antonietta Lucia
Brunetti, Francesca
Marazzato, Massimiliano
Longhi, Catia
Maurizi, Linda
Raponi, Giammarco
Palamara, Anna Teresa
Grassi, Sara
Conte, Maria Pia
author_facet Conte, Antonietta Lucia
Brunetti, Francesca
Marazzato, Massimiliano
Longhi, Catia
Maurizi, Linda
Raponi, Giammarco
Palamara, Anna Teresa
Grassi, Sara
Conte, Maria Pia
author_sort Conte, Antonietta Lucia
collection PubMed
description BACKGROUND: Atopic dermatitis (AD) is a chronic inflammatory skin condition whose pathogenesis involves genetic predisposition, epidermal barrier dysfunction, alterations in the immune responses and microbial dysbiosis. Clinical studies have shown a link between Staphylococcus aureus and the pathogenesis of AD, although the origins and genetic diversity of S. aureus colonizing patients with AD is poorly understood. The aim of the study was to investigate if specific clones might be associated with the disease. METHODS: WGS analyses were performed on 38 S. aureus strains, deriving from AD patients and healthy carriers. Genotypes (i.e. MLST, spa-, agr- and SCCmec-typing), genomic content (e.g. virulome and resistome), and the pan-genome structure of strains have been investigated. Phenotypic analyses were performed to determine the antibiotic susceptibility, the biofilm production and the invasiveness within the investigated S. aureus population. RESULTS: Strains isolated from AD patients revealed a high degree of genetic heterogeneity and a shared set of virulence factors and antimicrobial resistance genes, suggesting that no genotype and genomic content are uniquely associated with AD. The same strains were characterized by a lower variability in terms of gene content, indicating that the inflammatory conditions could exert a selective pressure leading to the optimization of the gene repertoire. Furthermore, genes related to specific mechanisms, like post-translational modification, protein turnover and chaperones as well as intracellular trafficking, secretion and vesicular transport, were significantly more enriched in AD strains. Phenotypic analysis revealed that all of our AD strains were strong or moderate biofilm producers, while less than half showed invasive capabilities. CONCLUSIONS: We conclude that in AD skin, the functional role played by S. aureus may depend on differential gene expression patterns and/or on post-translational modification mechanisms rather than being associated with peculiar genetic features.
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spelling pubmed-103031482023-06-29 Atopic dermatitis-derived Staphylococcus aureus strains: what makes them special in the interplay with the host Conte, Antonietta Lucia Brunetti, Francesca Marazzato, Massimiliano Longhi, Catia Maurizi, Linda Raponi, Giammarco Palamara, Anna Teresa Grassi, Sara Conte, Maria Pia Front Cell Infect Microbiol Cellular and Infection Microbiology BACKGROUND: Atopic dermatitis (AD) is a chronic inflammatory skin condition whose pathogenesis involves genetic predisposition, epidermal barrier dysfunction, alterations in the immune responses and microbial dysbiosis. Clinical studies have shown a link between Staphylococcus aureus and the pathogenesis of AD, although the origins and genetic diversity of S. aureus colonizing patients with AD is poorly understood. The aim of the study was to investigate if specific clones might be associated with the disease. METHODS: WGS analyses were performed on 38 S. aureus strains, deriving from AD patients and healthy carriers. Genotypes (i.e. MLST, spa-, agr- and SCCmec-typing), genomic content (e.g. virulome and resistome), and the pan-genome structure of strains have been investigated. Phenotypic analyses were performed to determine the antibiotic susceptibility, the biofilm production and the invasiveness within the investigated S. aureus population. RESULTS: Strains isolated from AD patients revealed a high degree of genetic heterogeneity and a shared set of virulence factors and antimicrobial resistance genes, suggesting that no genotype and genomic content are uniquely associated with AD. The same strains were characterized by a lower variability in terms of gene content, indicating that the inflammatory conditions could exert a selective pressure leading to the optimization of the gene repertoire. Furthermore, genes related to specific mechanisms, like post-translational modification, protein turnover and chaperones as well as intracellular trafficking, secretion and vesicular transport, were significantly more enriched in AD strains. Phenotypic analysis revealed that all of our AD strains were strong or moderate biofilm producers, while less than half showed invasive capabilities. CONCLUSIONS: We conclude that in AD skin, the functional role played by S. aureus may depend on differential gene expression patterns and/or on post-translational modification mechanisms rather than being associated with peculiar genetic features. Frontiers Media S.A. 2023-06-14 /pmc/articles/PMC10303148/ /pubmed/37389215 http://dx.doi.org/10.3389/fcimb.2023.1194254 Text en Copyright © 2023 Conte, Brunetti, Marazzato, Longhi, Maurizi, Raponi, Palamara, Grassi and Conte https://creativecommons.org/licenses/by/4.0/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.
spellingShingle Cellular and Infection Microbiology
Conte, Antonietta Lucia
Brunetti, Francesca
Marazzato, Massimiliano
Longhi, Catia
Maurizi, Linda
Raponi, Giammarco
Palamara, Anna Teresa
Grassi, Sara
Conte, Maria Pia
Atopic dermatitis-derived Staphylococcus aureus strains: what makes them special in the interplay with the host
title Atopic dermatitis-derived Staphylococcus aureus strains: what makes them special in the interplay with the host
title_full Atopic dermatitis-derived Staphylococcus aureus strains: what makes them special in the interplay with the host
title_fullStr Atopic dermatitis-derived Staphylococcus aureus strains: what makes them special in the interplay with the host
title_full_unstemmed Atopic dermatitis-derived Staphylococcus aureus strains: what makes them special in the interplay with the host
title_short Atopic dermatitis-derived Staphylococcus aureus strains: what makes them special in the interplay with the host
title_sort atopic dermatitis-derived staphylococcus aureus strains: what makes them special in the interplay with the host
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10303148/
https://www.ncbi.nlm.nih.gov/pubmed/37389215
http://dx.doi.org/10.3389/fcimb.2023.1194254
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