Staphylococcus aureus colonizing the skin microbiota of adults with severe atopic dermatitis exhibits genomic diversity and convergence in biofilm traits
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
Affiliations
Francesca Sivori
Microbiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, Italy
Ilaria Cavallo
Microbiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, Italy
Mauro Truglio
Microbiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, Italy
Flavio De Maio
Dipartimento di Scienze di Laboratorio e Infettivologiche, Fondazione Policlinico Universitario “A. Gemelli” IRCSS, Rome, Italy
Maurizio Sanguinetti
Dipartimento di Scienze di Laboratorio e Infettivologiche, Fondazione Policlinico Universitario “A. Gemelli” IRCSS, Rome, Italy
Giorgia Fabrizio
Department of Biology and Biotechnology “C. Darwin” Sapienza University of Rome, Rome, Italy
Valerio Licursi
Institute of Molecular Biology and Pathology, National Research Council of Italy, Rome, Italy
Massimo Francalancia
Microbiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, Italy
Fulvia Fraticelli
Microbiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, Italy
Ilenia La Greca
Microbiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, Italy
Federica Lucantoni
Department of Biology and Biotechnology “C. Darwin” Sapienza University of Rome, Rome, Italy
Emanuela Camera
Laboratory of Cutaneous Physiopathology and Integrated Center of Metabolomics Research, San Gallicano Dermatological Institute, IRCCS, Rome, Italy
Maria Mariano
Clinical Dermatology, San Gallicano Dermatological Institute, IRCCS, Rome, Italy
Fiorentina Ascenzioni
Department of Biology and Biotechnology “C. Darwin” Sapienza University of Rome, Rome, Italy
Antonio Cristaudo
Clinical Dermatology, San Gallicano Dermatological Institute, IRCCS, Rome, Italy
Fulvia Pimpinelli
Microbiology and Virology Unit, San Gallicano Dermatological Institute, IRCCS, Rome, Italy
Enea Gino Di Domenico
Microbiology 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.
