Altering the interfacial rheology of Pseudomonas aeruginosa and Staphylococcus aureus with N-acetyl cysteine and cysteamine

IntroductionChronic lung infection due to bacterial biofilms is one of the leading causes of mortality in cystic fibrosis (CF) patients. Among many species colonizing the lung airways, Pseudomonas aeruginosa and Staphylococcus aureus are two virulent pathogens involved in mechanically robust biofilm...

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Main Authors: Sricharani Rao Balmuri, Sena Noaman, Huda Usman, Tagbo H. R. Niepa
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2023.1338477/full
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author Sricharani Rao Balmuri
Sena Noaman
Huda Usman
Tagbo H. R. Niepa
Tagbo H. R. Niepa
Tagbo H. R. Niepa
Tagbo H. R. Niepa
Tagbo H. R. Niepa
author_facet Sricharani Rao Balmuri
Sena Noaman
Huda Usman
Tagbo H. R. Niepa
Tagbo H. R. Niepa
Tagbo H. R. Niepa
Tagbo H. R. Niepa
Tagbo H. R. Niepa
author_sort Sricharani Rao Balmuri
collection DOAJ
description IntroductionChronic lung infection due to bacterial biofilms is one of the leading causes of mortality in cystic fibrosis (CF) patients. Among many species colonizing the lung airways, Pseudomonas aeruginosa and Staphylococcus aureus are two virulent pathogens involved in mechanically robust biofilms that are difficult to eradicate using airway clearance techniques like lung lavage. To remove such biological materials, glycoside hydrolase-based compounds are commonly employed for targeting and breaking down the biofilm matrix, and subsequently increasing cell susceptibility to antibiotics.Materials and methodsIn this study, we evaluate the effects of N-acetyl cysteine (NAC) and Cysteamine (CYST) in disrupting interfacial bacterial films, targeting different components of the extracellular polymeric substances (EPS). We characterize the mechanics and structural integrity of the interfacial bacterial films using pendant drop elastometry and scanning electron microscopy.Results and discussionOur results show that the film architectures are compromised by treatment with disrupting agents for 6 h, which reduces film elasticity significantly. These effects are profound in the wild type and mucoid P. aeruginosa, compared to S. aureus. We further assess the effects of competition and cooperation between S. aureus and P. aeruginosa on the mechanics of composite interfacial films. Films of S. aureus and wild-type P. aeruginosa cocultures lose mechanical strength while those of S. aureus and mucoid P. aeruginosa exhibit improved storage modulus. Treatment with NAC and CYST reduces the elastic property of both composite films, owing to the drugs’ ability to disintegrate their EPS matrix. Overall, our results provide new insights into methods for assessing the efficacy of mucolytic agents against interfacial biofilms relevant to cystic fibrosis infection.
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spelling doaj.art-c97398a31bfa4f99a45ed39c9a9752af2024-01-16T04:26:37ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882024-01-011310.3389/fcimb.2023.13384771338477Altering the interfacial rheology of Pseudomonas aeruginosa and Staphylococcus aureus with N-acetyl cysteine and cysteamineSricharani Rao Balmuri0Sena Noaman1Huda Usman2Tagbo H. R. Niepa3Tagbo H. R. Niepa4Tagbo H. R. Niepa5Tagbo H. R. Niepa6Tagbo H. R. Niepa7Department of Chemical and Petroleum Engineering, Pittsburgh, PA, United StatesDepartment of Chemical and Petroleum Engineering, Pittsburgh, PA, United StatesDepartment of Chemical and Petroleum Engineering, Pittsburgh, PA, United StatesDepartment of Chemical and Petroleum Engineering, Pittsburgh, PA, United StatesCenter for Medicine and the Microbiome, Pittsburgh, PA, United StatesThe McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, PA, United StatesDepartment of Chemical Engineering, Pittsburgh, PA, United StatesDepartment of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, PA, United StatesIntroductionChronic lung infection due to bacterial biofilms is one of the leading causes of mortality in cystic fibrosis (CF) patients. Among many species colonizing the lung airways, Pseudomonas aeruginosa and Staphylococcus aureus are two virulent pathogens involved in mechanically robust biofilms that are difficult to eradicate using airway clearance techniques like lung lavage. To remove such biological materials, glycoside hydrolase-based compounds are commonly employed for targeting and breaking down the biofilm matrix, and subsequently increasing cell susceptibility to antibiotics.Materials and methodsIn this study, we evaluate the effects of N-acetyl cysteine (NAC) and Cysteamine (CYST) in disrupting interfacial bacterial films, targeting different components of the extracellular polymeric substances (EPS). We characterize the mechanics and structural integrity of the interfacial bacterial films using pendant drop elastometry and scanning electron microscopy.Results and discussionOur results show that the film architectures are compromised by treatment with disrupting agents for 6 h, which reduces film elasticity significantly. These effects are profound in the wild type and mucoid P. aeruginosa, compared to S. aureus. We further assess the effects of competition and cooperation between S. aureus and P. aeruginosa on the mechanics of composite interfacial films. Films of S. aureus and wild-type P. aeruginosa cocultures lose mechanical strength while those of S. aureus and mucoid P. aeruginosa exhibit improved storage modulus. Treatment with NAC and CYST reduces the elastic property of both composite films, owing to the drugs’ ability to disintegrate their EPS matrix. Overall, our results provide new insights into methods for assessing the efficacy of mucolytic agents against interfacial biofilms relevant to cystic fibrosis infection.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1338477/fullPseudomonas aeruginosaStaphylococcus aureusfluid interfacesthin-filminterfacial tension (IFT)viscoelastic materials
spellingShingle Sricharani Rao Balmuri
Sena Noaman
Huda Usman
Tagbo H. R. Niepa
Tagbo H. R. Niepa
Tagbo H. R. Niepa
Tagbo H. R. Niepa
Tagbo H. R. Niepa
Altering the interfacial rheology of Pseudomonas aeruginosa and Staphylococcus aureus with N-acetyl cysteine and cysteamine
Frontiers in Cellular and Infection Microbiology
Pseudomonas aeruginosa
Staphylococcus aureus
fluid interfaces
thin-film
interfacial tension (IFT)
viscoelastic materials
title Altering the interfacial rheology of Pseudomonas aeruginosa and Staphylococcus aureus with N-acetyl cysteine and cysteamine
title_full Altering the interfacial rheology of Pseudomonas aeruginosa and Staphylococcus aureus with N-acetyl cysteine and cysteamine
title_fullStr Altering the interfacial rheology of Pseudomonas aeruginosa and Staphylococcus aureus with N-acetyl cysteine and cysteamine
title_full_unstemmed Altering the interfacial rheology of Pseudomonas aeruginosa and Staphylococcus aureus with N-acetyl cysteine and cysteamine
title_short Altering the interfacial rheology of Pseudomonas aeruginosa and Staphylococcus aureus with N-acetyl cysteine and cysteamine
title_sort altering the interfacial rheology of pseudomonas aeruginosa and staphylococcus aureus with n acetyl cysteine and cysteamine
topic Pseudomonas aeruginosa
Staphylococcus aureus
fluid interfaces
thin-film
interfacial tension (IFT)
viscoelastic materials
url https://www.frontiersin.org/articles/10.3389/fcimb.2023.1338477/full
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