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The Transcription Factor SpoVG Is of Major Importance for Biofilm Formation of Staphylococcus epidermidis under In Vitro Conditions, but Dispensable for In Vivo Biofilm Formation

Staphylococcus epidermidis is a common cause of device related infections on which pathogens form biofilms (i.e., multilayered cell populations embedded in an extracellular matrix). Here, we report that the transcription factor SpoVG is essential for the capacity of S. epidermidis to form such biofi...

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Autores principales: Benthien, Hannah, Fresenborg, Beate, Pätzold, Linda, Elhawy, Mohamed Ibrahem, Huc-Brandt, Sylvaine, Beisswenger, Christoph, Krasteva-Christ, Gabriela, Becker, Sören L., Molle, Virginie, Knobloch, Johannes K., Bischoff, Markus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8949118/
https://www.ncbi.nlm.nih.gov/pubmed/35328675
http://dx.doi.org/10.3390/ijms23063255
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author Benthien, Hannah
Fresenborg, Beate
Pätzold, Linda
Elhawy, Mohamed Ibrahem
Huc-Brandt, Sylvaine
Beisswenger, Christoph
Krasteva-Christ, Gabriela
Becker, Sören L.
Molle, Virginie
Knobloch, Johannes K.
Bischoff, Markus
author_facet Benthien, Hannah
Fresenborg, Beate
Pätzold, Linda
Elhawy, Mohamed Ibrahem
Huc-Brandt, Sylvaine
Beisswenger, Christoph
Krasteva-Christ, Gabriela
Becker, Sören L.
Molle, Virginie
Knobloch, Johannes K.
Bischoff, Markus
author_sort Benthien, Hannah
collection PubMed
description Staphylococcus epidermidis is a common cause of device related infections on which pathogens form biofilms (i.e., multilayered cell populations embedded in an extracellular matrix). Here, we report that the transcription factor SpoVG is essential for the capacity of S. epidermidis to form such biofilms on artificial surfaces under in vitro conditions. Inactivation of spoVG in the polysaccharide intercellular adhesin (PIA) producing S. epidermidis strain 1457 yielded a mutant that, unlike its parental strain, failed to produce a clear biofilm in a microtiter plate-based static biofilm assay. A decreased biofilm formation capacity was also observed when 1457 ΔspoVG cells were co-cultured with polyurethane-based peripheral venous catheter fragments under dynamic conditions, while the cis-complemented 1457 ΔspoVG::spoVG derivative formed biofilms comparable to the levels seen with the wild-type. Transcriptional studies demonstrated that the deletion of spoVG significantly altered the expression of the intercellular adhesion (ica) locus by upregulating the transcription of the ica operon repressor icaR and down-regulating the transcription of icaADBC. Electrophoretic mobility shift assays (EMSA) revealed an interaction between SpoVG and the icaA-icaR intergenic region, suggesting SpoVG to promote biofilm formation of S. epidermidis by modulating ica expression. However, when mice were challenged with the 1457 ΔspoVG mutant in a foreign body infection model, only marginal differences in biomasses produced on the infected catheter fragments between the mutant and the parental strain were observed. These findings suggest that SpoVG is critical for the PIA-dependent biofilm formation of S. epidermis under in vitro conditions, but is largely dispensable for biofilm formation of this skin commensal under in vivo conditions.
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spelling pubmed-89491182022-03-26 The Transcription Factor SpoVG Is of Major Importance for Biofilm Formation of Staphylococcus epidermidis under In Vitro Conditions, but Dispensable for In Vivo Biofilm Formation Benthien, Hannah Fresenborg, Beate Pätzold, Linda Elhawy, Mohamed Ibrahem Huc-Brandt, Sylvaine Beisswenger, Christoph Krasteva-Christ, Gabriela Becker, Sören L. Molle, Virginie Knobloch, Johannes K. Bischoff, Markus Int J Mol Sci Article Staphylococcus epidermidis is a common cause of device related infections on which pathogens form biofilms (i.e., multilayered cell populations embedded in an extracellular matrix). Here, we report that the transcription factor SpoVG is essential for the capacity of S. epidermidis to form such biofilms on artificial surfaces under in vitro conditions. Inactivation of spoVG in the polysaccharide intercellular adhesin (PIA) producing S. epidermidis strain 1457 yielded a mutant that, unlike its parental strain, failed to produce a clear biofilm in a microtiter plate-based static biofilm assay. A decreased biofilm formation capacity was also observed when 1457 ΔspoVG cells were co-cultured with polyurethane-based peripheral venous catheter fragments under dynamic conditions, while the cis-complemented 1457 ΔspoVG::spoVG derivative formed biofilms comparable to the levels seen with the wild-type. Transcriptional studies demonstrated that the deletion of spoVG significantly altered the expression of the intercellular adhesion (ica) locus by upregulating the transcription of the ica operon repressor icaR and down-regulating the transcription of icaADBC. Electrophoretic mobility shift assays (EMSA) revealed an interaction between SpoVG and the icaA-icaR intergenic region, suggesting SpoVG to promote biofilm formation of S. epidermidis by modulating ica expression. However, when mice were challenged with the 1457 ΔspoVG mutant in a foreign body infection model, only marginal differences in biomasses produced on the infected catheter fragments between the mutant and the parental strain were observed. These findings suggest that SpoVG is critical for the PIA-dependent biofilm formation of S. epidermis under in vitro conditions, but is largely dispensable for biofilm formation of this skin commensal under in vivo conditions. MDPI 2022-03-17 /pmc/articles/PMC8949118/ /pubmed/35328675 http://dx.doi.org/10.3390/ijms23063255 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Benthien, Hannah
Fresenborg, Beate
Pätzold, Linda
Elhawy, Mohamed Ibrahem
Huc-Brandt, Sylvaine
Beisswenger, Christoph
Krasteva-Christ, Gabriela
Becker, Sören L.
Molle, Virginie
Knobloch, Johannes K.
Bischoff, Markus
The Transcription Factor SpoVG Is of Major Importance for Biofilm Formation of Staphylococcus epidermidis under In Vitro Conditions, but Dispensable for In Vivo Biofilm Formation
title The Transcription Factor SpoVG Is of Major Importance for Biofilm Formation of Staphylococcus epidermidis under In Vitro Conditions, but Dispensable for In Vivo Biofilm Formation
title_full The Transcription Factor SpoVG Is of Major Importance for Biofilm Formation of Staphylococcus epidermidis under In Vitro Conditions, but Dispensable for In Vivo Biofilm Formation
title_fullStr The Transcription Factor SpoVG Is of Major Importance for Biofilm Formation of Staphylococcus epidermidis under In Vitro Conditions, but Dispensable for In Vivo Biofilm Formation
title_full_unstemmed The Transcription Factor SpoVG Is of Major Importance for Biofilm Formation of Staphylococcus epidermidis under In Vitro Conditions, but Dispensable for In Vivo Biofilm Formation
title_short The Transcription Factor SpoVG Is of Major Importance for Biofilm Formation of Staphylococcus epidermidis under In Vitro Conditions, but Dispensable for In Vivo Biofilm Formation
title_sort transcription factor spovg is of major importance for biofilm formation of staphylococcus epidermidis under in vitro conditions, but dispensable for in vivo biofilm formation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8949118/
https://www.ncbi.nlm.nih.gov/pubmed/35328675
http://dx.doi.org/10.3390/ijms23063255
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