Staphylococcus aureus colonizing the skin microbiota of adults with severe atopic dermatitis exhibits genomic diversity and convergence in biofilm traits
Atopic dermatitis (AD) is a chronic inflammatory skin disorder exacerbated by Staphylococcus aureus colonization. The specific factors that drive S. aureus overgrowth and persistence in AD remain poorly understood. This study analyzed skin barrier functions and microbiome diversity in lesional (LE)...
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Elsevier
2024-12-01
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| Series: | Biofilm |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2590207524000479 |
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| author | Francesca Sivori Ilaria Cavallo Mauro Truglio Flavio De Maio Maurizio Sanguinetti Giorgia Fabrizio Valerio Licursi Massimo Francalancia Fulvia Fraticelli Ilenia La Greca Federica Lucantoni Emanuela Camera Maria Mariano Fiorentina Ascenzioni Antonio Cristaudo Fulvia Pimpinelli Enea Gino Di Domenico |
| author_facet | Francesca Sivori Ilaria Cavallo Mauro Truglio Flavio De Maio Maurizio Sanguinetti Giorgia Fabrizio Valerio Licursi Massimo Francalancia Fulvia Fraticelli Ilenia La Greca Federica Lucantoni Emanuela Camera Maria Mariano Fiorentina Ascenzioni Antonio Cristaudo Fulvia Pimpinelli Enea Gino Di Domenico |
| author_sort | Francesca Sivori |
| collection | DOAJ |
| description | Atopic dermatitis (AD) is a chronic inflammatory skin disorder exacerbated by Staphylococcus aureus colonization. The specific factors that drive S. aureus overgrowth and persistence in AD remain poorly understood. This study analyzed skin barrier functions and microbiome diversity in lesional (LE) and non-lesional (NL) forearm sites of individuals with severe AD compared to healthy control subjects (HS). Notable differences were found in transepidermal water loss, stratum corneum hydration, and microbiome composition. Cutibacterium was more prevalent in HS, while S. aureus and S. lugdunensis were predominantly found in AD LE skin. The results highlighted that microbial balance depends on inter-species competition. Specifically, network analysis at the genus level demonstrated that overall bacterial correlations were higher in HS, indicating a more stable microbial community. Notably, network analysis at the species level revealed that S. aureus engaged in competitive interactions in NL and LE but not in HS. Whole-genome sequencing (WGS) showed considerable genetic diversity among S. aureus strains from AD. Despite this variability, the isolates exhibited convergence in key phenotypic traits such as adhesion and biofilm formation, which are crucial for microbial persistence. These common phenotypes suggest an adaptive evolution, driven by competition in the AD skin microenvironment, of S. aureus and underscoring the interplay between genetic diversity and phenotypic convergence in microbial adaptation. |
| format | Article |
| id | doaj-art-9b497d4a6cdf4d20bbc2c63e34bb3d77 |
| institution | DOAJ |
| issn | 2590-2075 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Biofilm |
| spelling | doaj-art-9b497d4a6cdf4d20bbc2c63e34bb3d772025-08-20T02:39:27ZengElsevierBiofilm2590-20752024-12-01810022210.1016/j.bioflm.2024.100222Staphylococcus aureus colonizing the skin microbiota of adults with severe atopic dermatitis exhibits genomic diversity and convergence in biofilm traitsFrancesca Sivori0Ilaria Cavallo1Mauro Truglio2Flavio De Maio3Maurizio Sanguinetti4Giorgia Fabrizio5Valerio Licursi6Massimo Francalancia7Fulvia Fraticelli8Ilenia La Greca9Federica Lucantoni10Emanuela Camera11Maria Mariano12Fiorentina Ascenzioni13Antonio Cristaudo14Fulvia Pimpinelli15Enea Gino Di Domenico16Microbiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, ItalyMicrobiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, ItalyMicrobiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, ItalyDipartimento di Scienze di Laboratorio e Infettivologiche, Fondazione Policlinico Universitario “A. Gemelli” IRCSS, Rome, ItalyDipartimento di Scienze di Laboratorio e Infettivologiche, Fondazione Policlinico Universitario “A. Gemelli” IRCSS, Rome, ItalyDepartment of Biology and Biotechnology “C. Darwin” Sapienza University of Rome, Rome, ItalyInstitute of Molecular Biology and Pathology, National Research Council of Italy, Rome, ItalyMicrobiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, ItalyMicrobiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, ItalyMicrobiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, ItalyDepartment of Biology and Biotechnology “C. Darwin” Sapienza University of Rome, Rome, ItalyLaboratory of Cutaneous Physiopathology and Integrated Center of Metabolomics Research, San Gallicano Dermatological Institute, IRCCS, Rome, ItalyClinical Dermatology, San Gallicano Dermatological Institute, IRCCS, Rome, ItalyDepartment of Biology and Biotechnology “C. Darwin” Sapienza University of Rome, Rome, ItalyClinical Dermatology, San Gallicano Dermatological Institute, IRCCS, Rome, ItalyMicrobiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, ItalyMicrobiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, Italy; Corresponding author.Atopic dermatitis (AD) is a chronic inflammatory skin disorder exacerbated by Staphylococcus aureus colonization. The specific factors that drive S. aureus overgrowth and persistence in AD remain poorly understood. This study analyzed skin barrier functions and microbiome diversity in lesional (LE) and non-lesional (NL) forearm sites of individuals with severe AD compared to healthy control subjects (HS). Notable differences were found in transepidermal water loss, stratum corneum hydration, and microbiome composition. Cutibacterium was more prevalent in HS, while S. aureus and S. lugdunensis were predominantly found in AD LE skin. The results highlighted that microbial balance depends on inter-species competition. Specifically, network analysis at the genus level demonstrated that overall bacterial correlations were higher in HS, indicating a more stable microbial community. Notably, network analysis at the species level revealed that S. aureus engaged in competitive interactions in NL and LE but not in HS. Whole-genome sequencing (WGS) showed considerable genetic diversity among S. aureus strains from AD. Despite this variability, the isolates exhibited convergence in key phenotypic traits such as adhesion and biofilm formation, which are crucial for microbial persistence. These common phenotypes suggest an adaptive evolution, driven by competition in the AD skin microenvironment, of S. aureus and underscoring the interplay between genetic diversity and phenotypic convergence in microbial adaptation.http://www.sciencedirect.com/science/article/pii/S2590207524000479Atopic dermatitisSkinMicrobiomeStaphylococcus aureusBiofilmMRSA |
| spellingShingle | Francesca Sivori Ilaria Cavallo Mauro Truglio Flavio De Maio Maurizio Sanguinetti Giorgia Fabrizio Valerio Licursi Massimo Francalancia Fulvia Fraticelli Ilenia La Greca Federica Lucantoni Emanuela Camera Maria Mariano Fiorentina Ascenzioni Antonio Cristaudo Fulvia Pimpinelli Enea Gino Di Domenico Staphylococcus aureus colonizing the skin microbiota of adults with severe atopic dermatitis exhibits genomic diversity and convergence in biofilm traits Biofilm Atopic dermatitis Skin Microbiome Staphylococcus aureus Biofilm MRSA |
| title | Staphylococcus aureus colonizing the skin microbiota of adults with severe atopic dermatitis exhibits genomic diversity and convergence in biofilm traits |
| title_full | Staphylococcus aureus colonizing the skin microbiota of adults with severe atopic dermatitis exhibits genomic diversity and convergence in biofilm traits |
| title_fullStr | Staphylococcus aureus colonizing the skin microbiota of adults with severe atopic dermatitis exhibits genomic diversity and convergence in biofilm traits |
| title_full_unstemmed | Staphylococcus aureus colonizing the skin microbiota of adults with severe atopic dermatitis exhibits genomic diversity and convergence in biofilm traits |
| title_short | Staphylococcus aureus colonizing the skin microbiota of adults with severe atopic dermatitis exhibits genomic diversity and convergence in biofilm traits |
| title_sort | staphylococcus aureus colonizing the skin microbiota of adults with severe atopic dermatitis exhibits genomic diversity and convergence in biofilm traits |
| topic | Atopic dermatitis Skin Microbiome Staphylococcus aureus Biofilm MRSA |
| url | http://www.sciencedirect.com/science/article/pii/S2590207524000479 |
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