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Adaptation of Staphylococcus aureus to the Human Skin Environment Identified Using an ex vivo Tissue Model

The healthy human epidermis provides physical protection and is impenetrable for pathogenic microbes. Nevertheless, commensal and pathogen bacteria such as Staphylococcus aureus are able to colonize the skin surface, which may subsequently lead to infection. To identify and characterize regulatory e...

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Autores principales: Burian, Marc, Plange, Johanna, Schmitt, Laurenz, Kaschke, Anke, Marquardt, Yvonne, Huth, Laura, Baron, Jens M., Hornef, Mathias W., Wolz, Christiane, Yazdi, Amir S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8490888/
https://www.ncbi.nlm.nih.gov/pubmed/34621255
http://dx.doi.org/10.3389/fmicb.2021.728989
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author Burian, Marc
Plange, Johanna
Schmitt, Laurenz
Kaschke, Anke
Marquardt, Yvonne
Huth, Laura
Baron, Jens M.
Hornef, Mathias W.
Wolz, Christiane
Yazdi, Amir S.
author_facet Burian, Marc
Plange, Johanna
Schmitt, Laurenz
Kaschke, Anke
Marquardt, Yvonne
Huth, Laura
Baron, Jens M.
Hornef, Mathias W.
Wolz, Christiane
Yazdi, Amir S.
author_sort Burian, Marc
collection PubMed
description The healthy human epidermis provides physical protection and is impenetrable for pathogenic microbes. Nevertheless, commensal and pathogen bacteria such as Staphylococcus aureus are able to colonize the skin surface, which may subsequently lead to infection. To identify and characterize regulatory elements facilitating adaptation of S. aureus to the human skin environment we used ex vivo tissue explants and quantified S. aureus gene transcription during co-culture. This analysis provided evidence for a significant downregulation of the global virulence regulator agr upon initial contact with skin, regardless of the growth phase of S. aureus prior to co-culture. In contrast, the alternative sigma factor B (sigB) and the antimicrobial peptide-sensing system (graRS) were expressed during early colonization. Consistently, sigB target genes such as the clumping factor A (clfA) and fibrinogen and fibronectin binding protein A (fnbA) were strongly upregulated upon skin contact. At later timepoints of the adhesion process, wall teichoic acid (WTA) synthesis was induced. Besides the expression of adhesive molecules, transcription of molecules involved in immune evasion were increased during late colonization (staphylococcal complement inhibitor and staphylokinase). Similar to nasal colonization, enzymes involved in cell wall metabolism (sceD and atlA) were highly transcribed. Finally, we detected a strong expression of proteases from all three catalytic classes during the entire colonization process. Taken together, we here present an ex vivo skin colonization model that allows the detailed characterization of the bacterial adaptation to the skin environment.
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spelling pubmed-84908882021-10-06 Adaptation of Staphylococcus aureus to the Human Skin Environment Identified Using an ex vivo Tissue Model Burian, Marc Plange, Johanna Schmitt, Laurenz Kaschke, Anke Marquardt, Yvonne Huth, Laura Baron, Jens M. Hornef, Mathias W. Wolz, Christiane Yazdi, Amir S. Front Microbiol Microbiology The healthy human epidermis provides physical protection and is impenetrable for pathogenic microbes. Nevertheless, commensal and pathogen bacteria such as Staphylococcus aureus are able to colonize the skin surface, which may subsequently lead to infection. To identify and characterize regulatory elements facilitating adaptation of S. aureus to the human skin environment we used ex vivo tissue explants and quantified S. aureus gene transcription during co-culture. This analysis provided evidence for a significant downregulation of the global virulence regulator agr upon initial contact with skin, regardless of the growth phase of S. aureus prior to co-culture. In contrast, the alternative sigma factor B (sigB) and the antimicrobial peptide-sensing system (graRS) were expressed during early colonization. Consistently, sigB target genes such as the clumping factor A (clfA) and fibrinogen and fibronectin binding protein A (fnbA) were strongly upregulated upon skin contact. At later timepoints of the adhesion process, wall teichoic acid (WTA) synthesis was induced. Besides the expression of adhesive molecules, transcription of molecules involved in immune evasion were increased during late colonization (staphylococcal complement inhibitor and staphylokinase). Similar to nasal colonization, enzymes involved in cell wall metabolism (sceD and atlA) were highly transcribed. Finally, we detected a strong expression of proteases from all three catalytic classes during the entire colonization process. Taken together, we here present an ex vivo skin colonization model that allows the detailed characterization of the bacterial adaptation to the skin environment. Frontiers Media S.A. 2021-09-21 /pmc/articles/PMC8490888/ /pubmed/34621255 http://dx.doi.org/10.3389/fmicb.2021.728989 Text en Copyright © 2021 Burian, Plange, Schmitt, Kaschke, Marquardt, Huth, Baron, Hornef, Wolz and Yazdi. 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 Microbiology
Burian, Marc
Plange, Johanna
Schmitt, Laurenz
Kaschke, Anke
Marquardt, Yvonne
Huth, Laura
Baron, Jens M.
Hornef, Mathias W.
Wolz, Christiane
Yazdi, Amir S.
Adaptation of Staphylococcus aureus to the Human Skin Environment Identified Using an ex vivo Tissue Model
title Adaptation of Staphylococcus aureus to the Human Skin Environment Identified Using an ex vivo Tissue Model
title_full Adaptation of Staphylococcus aureus to the Human Skin Environment Identified Using an ex vivo Tissue Model
title_fullStr Adaptation of Staphylococcus aureus to the Human Skin Environment Identified Using an ex vivo Tissue Model
title_full_unstemmed Adaptation of Staphylococcus aureus to the Human Skin Environment Identified Using an ex vivo Tissue Model
title_short Adaptation of Staphylococcus aureus to the Human Skin Environment Identified Using an ex vivo Tissue Model
title_sort adaptation of staphylococcus aureus to the human skin environment identified using an ex vivo tissue model
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8490888/
https://www.ncbi.nlm.nih.gov/pubmed/34621255
http://dx.doi.org/10.3389/fmicb.2021.728989
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