Microstructural and Rheological Transitions in Bacterial Biofilms

Abstract Biofilms are aggregated bacterial communities structured within an extracellular matrix (ECM). ECM controls biofilm architecture and confers mechanical resistance against shear forces. From a physical perspective, biofilms can be described as colloidal gels, where bacterial cells are analog...

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Main Authors: Samuel G.V. Charlton, Amber N. Bible, Eleonora Secchi, Jennifer L. Morrell‐Falvey, Scott T. Retterer, Thomas P. Curtis, Jinju Chen, Saikat Jana
Format: Article
Language:English
Published: Wiley 2023-09-01
Series:Advanced Science
Subjects:
Online Access:https://doi.org/10.1002/advs.202207373
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author Samuel G.V. Charlton
Amber N. Bible
Eleonora Secchi
Jennifer L. Morrell‐Falvey
Scott T. Retterer
Thomas P. Curtis
Jinju Chen
Saikat Jana
author_facet Samuel G.V. Charlton
Amber N. Bible
Eleonora Secchi
Jennifer L. Morrell‐Falvey
Scott T. Retterer
Thomas P. Curtis
Jinju Chen
Saikat Jana
author_sort Samuel G.V. Charlton
collection DOAJ
description Abstract Biofilms are aggregated bacterial communities structured within an extracellular matrix (ECM). ECM controls biofilm architecture and confers mechanical resistance against shear forces. From a physical perspective, biofilms can be described as colloidal gels, where bacterial cells are analogous to colloidal particles distributed in the polymeric ECM. However, the influence of the ECM in altering the cellular packing fraction (ϕ) and the resulting viscoelastic behavior of biofilm remains unexplored. Using biofilms of Pantoea sp. (WT) and its mutant (ΔUDP), the correlation between biofilm structure and its viscoelastic response is investigated. Experiments show that the reduction of exopolysaccharide production in ΔUDP biofilms corresponds with a seven‐fold increase in ϕ, resulting in a colloidal glass‐like structure. Consequently, the rheological signatures become altered, with the WT behaving like a weak gel, whilst the ΔUDP displayed a glass‐like rheological signature. By co‐culturing the two strains, biofilm ϕ is modulated which allows us to explore the structural changes and capture a change in viscoelastic response from a weak to a strong gel, and to a colloidal glass‐like state. The results reveal the role of exopolysaccharide in mediating a structural transition in biofilms and demonstrate a correlation between biofilm structure and viscoelastic response.
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spelling doaj.art-4bea714791ed4adc9e90042680cdbc422023-09-26T07:39:32ZengWileyAdvanced Science2198-38442023-09-011027n/an/a10.1002/advs.202207373Microstructural and Rheological Transitions in Bacterial BiofilmsSamuel G.V. Charlton0Amber N. Bible1Eleonora Secchi2Jennifer L. Morrell‐Falvey3Scott T. Retterer4Thomas P. Curtis5Jinju Chen6Saikat Jana7Department of Civil, Environmental and Geomatic Engineering Institute of Environmental Engineering ETH Zurich Zurich 8049 SwitzerlandBiosciences Division Oak Ridge National Laboratory Oak Ridge TN 37830 USADepartment of Civil, Environmental and Geomatic Engineering Institute of Environmental Engineering ETH Zurich Zurich 8049 SwitzerlandBiosciences Division Oak Ridge National Laboratory Oak Ridge TN 37830 USABiosciences Division Oak Ridge National Laboratory Oak Ridge TN 37830 USASchool of Engineering Newcastle University Newcastle Upon Tyne NE1 7RU UKSchool of Engineering Newcastle University Newcastle Upon Tyne NE1 7RU UKSchool of Engineering Newcastle University Newcastle Upon Tyne NE1 7RU UKAbstract Biofilms are aggregated bacterial communities structured within an extracellular matrix (ECM). ECM controls biofilm architecture and confers mechanical resistance against shear forces. From a physical perspective, biofilms can be described as colloidal gels, where bacterial cells are analogous to colloidal particles distributed in the polymeric ECM. However, the influence of the ECM in altering the cellular packing fraction (ϕ) and the resulting viscoelastic behavior of biofilm remains unexplored. Using biofilms of Pantoea sp. (WT) and its mutant (ΔUDP), the correlation between biofilm structure and its viscoelastic response is investigated. Experiments show that the reduction of exopolysaccharide production in ΔUDP biofilms corresponds with a seven‐fold increase in ϕ, resulting in a colloidal glass‐like structure. Consequently, the rheological signatures become altered, with the WT behaving like a weak gel, whilst the ΔUDP displayed a glass‐like rheological signature. By co‐culturing the two strains, biofilm ϕ is modulated which allows us to explore the structural changes and capture a change in viscoelastic response from a weak to a strong gel, and to a colloidal glass‐like state. The results reveal the role of exopolysaccharide in mediating a structural transition in biofilms and demonstrate a correlation between biofilm structure and viscoelastic response.https://doi.org/10.1002/advs.202207373biofilmsextracellular exopolysaccharidespacking fractionPayne effectviscoelasticity
spellingShingle Samuel G.V. Charlton
Amber N. Bible
Eleonora Secchi
Jennifer L. Morrell‐Falvey
Scott T. Retterer
Thomas P. Curtis
Jinju Chen
Saikat Jana
Microstructural and Rheological Transitions in Bacterial Biofilms
Advanced Science
biofilms
extracellular exopolysaccharides
packing fraction
Payne effect
viscoelasticity
title Microstructural and Rheological Transitions in Bacterial Biofilms
title_full Microstructural and Rheological Transitions in Bacterial Biofilms
title_fullStr Microstructural and Rheological Transitions in Bacterial Biofilms
title_full_unstemmed Microstructural and Rheological Transitions in Bacterial Biofilms
title_short Microstructural and Rheological Transitions in Bacterial Biofilms
title_sort microstructural and rheological transitions in bacterial biofilms
topic biofilms
extracellular exopolysaccharides
packing fraction
Payne effect
viscoelasticity
url https://doi.org/10.1002/advs.202207373
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