Physical mechanisms driving the reversible aggregation of Staphylococcus aureus and response to antimicrobials

Abstract Formation of non-sessile, auto-aggregated cells of Staphylococcus aureus contributes to surface colonization and biofilm formation, hence play a major role in the early establishment of infection and in tolerance to antimicrobials. Understanding the mechanism of aggregation and the impact o...

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Main Authors: Céline Burel, Rémi Dreyfus, Laura Purevdorj-Gage
Format: Article
Language:English
Published: Nature Publishing Group 2021-07-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-94457-1
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spelling doaj-8c1c8fe0026348b0827e6fe1512e169d2021-07-25T11:24:01ZengNature Publishing GroupScientific Reports2045-23222021-07-011111910.1038/s41598-021-94457-1Physical mechanisms driving the reversible aggregation of Staphylococcus aureus and response to antimicrobialsCéline Burel0Rémi Dreyfus1Laura Purevdorj-Gage2Complex Assemblies of Soft Matter Laboratory (COMPASS), IRL 3254, CNRS-Solvay-University of Pennsylvania, CRTBComplex Assemblies of Soft Matter Laboratory (COMPASS), IRL 3254, CNRS-Solvay-University of Pennsylvania, CRTBSolvay, Novecare CRTBAbstract Formation of non-sessile, auto-aggregated cells of Staphylococcus aureus contributes to surface colonization and biofilm formation, hence play a major role in the early establishment of infection and in tolerance to antimicrobials. Understanding the mechanism of aggregation and the impact of aggregation on the activity of antimicrobials is crucial in achieving a better control of this important pathogen. Previously linked to biological phenomena, physical interactions leading to S. aureus cellular aggregation and its protective features against antimicrobials remain unraveled. Herein, in-vitro experiments coupled with XDLVO simulations reveal that suspensions of S. aureus cells exhibit rapid, reversible aggregation (> 70%) in part controlled by the interplay between cellular hydrophobicity, surface potential and extracellular proteins. Changing pH and salt concentration in the extracellular media modulated the cellular surface potential but not the hydrophobicity which remained consistent despite these variations. A decrease in net cellular negative surface potential achieved by decreasing pH or increasing salt concentrations, caused attractive forces such as the hydrophobic and cell–protein interactions to prevail, favoring immediate aggregation. The aggregation significantly increased the tolerance of S. aureus cells to quaternary ammonium compounds (QAC). The well-dispersed cell population was completely inactivated within 30 s whereas its aggregated counterpart required more than 10 min.https://doi.org/10.1038/s41598-021-94457-1
collection DOAJ
language English
format Article
sources DOAJ
author Céline Burel
Rémi Dreyfus
Laura Purevdorj-Gage
spellingShingle Céline Burel
Rémi Dreyfus
Laura Purevdorj-Gage
Physical mechanisms driving the reversible aggregation of Staphylococcus aureus and response to antimicrobials
Scientific Reports
author_facet Céline Burel
Rémi Dreyfus
Laura Purevdorj-Gage
author_sort Céline Burel
title Physical mechanisms driving the reversible aggregation of Staphylococcus aureus and response to antimicrobials
title_short Physical mechanisms driving the reversible aggregation of Staphylococcus aureus and response to antimicrobials
title_full Physical mechanisms driving the reversible aggregation of Staphylococcus aureus and response to antimicrobials
title_fullStr Physical mechanisms driving the reversible aggregation of Staphylococcus aureus and response to antimicrobials
title_full_unstemmed Physical mechanisms driving the reversible aggregation of Staphylococcus aureus and response to antimicrobials
title_sort physical mechanisms driving the reversible aggregation of staphylococcus aureus and response to antimicrobials
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2021-07-01
description Abstract Formation of non-sessile, auto-aggregated cells of Staphylococcus aureus contributes to surface colonization and biofilm formation, hence play a major role in the early establishment of infection and in tolerance to antimicrobials. Understanding the mechanism of aggregation and the impact of aggregation on the activity of antimicrobials is crucial in achieving a better control of this important pathogen. Previously linked to biological phenomena, physical interactions leading to S. aureus cellular aggregation and its protective features against antimicrobials remain unraveled. Herein, in-vitro experiments coupled with XDLVO simulations reveal that suspensions of S. aureus cells exhibit rapid, reversible aggregation (> 70%) in part controlled by the interplay between cellular hydrophobicity, surface potential and extracellular proteins. Changing pH and salt concentration in the extracellular media modulated the cellular surface potential but not the hydrophobicity which remained consistent despite these variations. A decrease in net cellular negative surface potential achieved by decreasing pH or increasing salt concentrations, caused attractive forces such as the hydrophobic and cell–protein interactions to prevail, favoring immediate aggregation. The aggregation significantly increased the tolerance of S. aureus cells to quaternary ammonium compounds (QAC). The well-dispersed cell population was completely inactivated within 30 s whereas its aggregated counterpart required more than 10 min.
url https://doi.org/10.1038/s41598-021-94457-1
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