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

Antonietta Lucia Conte; Francesca Brunetti; Massimiliano Marazzato; Catia Longhi; Linda Maurizi; Giammarco Raponi; Anna Teresa Palamara; Sara Grassi; Maria Pia Conte

doi:10.3389/fcimb.2023.1194254

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

Front Cell Infect Microbiol. 2023 Jun 14:13:1194254. doi: 10.3389/fcimb.2023.1194254. eCollection 2023.

Authors

Antonietta Lucia Conte¹, Francesca Brunetti¹, Massimiliano Marazzato¹, Catia Longhi¹, Linda Maurizi¹, Giammarco Raponi¹, Anna Teresa Palamara^{2

3}, Sara Grassi⁴, Maria Pia Conte¹

Affiliations

¹ Department of Public Health and Infectious Diseases, Sapienza University of Rome, Rome, Italy.
² Department of Infectious Diseases, Istituto Superiore di Sanità, Rome, Italy.
³ Department of Public Health and Infectious Diseases, Sapienza University of Rome, Laboratory Affiliated to Institute Pasteur Italia- Cenci Bolognetti Foundation, Rome, Italy.
⁴ Dermatology Clinic, Department of Clinical Internal, Anesthesiological and Cardiovascular Sciences, Sapienza University of Rome, Rome, Italy.

Abstract

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.

Keywords: Staphylococcus aureus; antibiotic resistance; atopic dermatitis; biofilm; in silico genotype; pan-genome; whole-genome sequencing.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Dermatitis, Atopic*
Genotype
Humans
Multilocus Sequence Typing
Skin
Staphylococcus aureus / genetics

Grants and funding

This work was supported by Ateneo Grant 2018, RG1181642C2C4B17. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.