Microstructural and Rheological Transitions in Bacterial Biofilms

Samuel G.V. Charlton; Amber N. Bible; Eleonora Secchi; Jennifer L. Morrell‐Falvey; Scott T. Retterer; Thomas P. Curtis; Jinju Chen; Saikat Jana

doi:10.1002/advs.202207373

Microstructural and Rheological Transitions in Bacterial Biofilms

Samuel G.V. Charlton, Amber N. Bible, Eleonora Secchi, Jennifer L. Morrell‐Falvey, Scott T. Retterer, Thomas P. Curtis, Jinju Chen, Saikat Jana

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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.

Original language	English
Pages (from-to)	1-11
Number of pages	12
Journal	Advanced Science
Volume	10
Issue number	27
Early online date	31 Jul 2023
DOIs	https://doi.org/10.1002/advs.202207373
Publication status	Published online - 31 Jul 2023

Bibliographical note

Funding Information:
T.P.C. and J.C. acknowledge funding from Engineering and Physical Sciences Research Council (UK) through award number EP/K039083/1 to Newcastle University. S.G.V.C. acknowledges the EPSRC DTP studentship from Newcastle University. J.L.M., A.N.B., and S.T.R. acknowledge funding from the Genomic Science Program, U.S. Department of Energy, Office of Science, Biological and Environmental Research, as part of the Plant‐Microbe Interfaces Scientific Focus Area. E.S. acknowledges funding from the SNSF PRIMA grant 179834. This research used resources of the Center for Nanophase Materials Sciences, which was a US Department of Energy, Office of Science User Facility at Oak Ridge National Laboratory. Oak Ridge National Laboratory is managed by UT‐Battelle, LLC, for the U.S. Department of Energy under contract DE‐AC05‐00OR22725. The authors thank Prof. A. Wipat, Prof. J.G. Burgess and Dr. Lucy E. Eland for encouraging discussions and providing access to their laboratories. Assistance from members of the Bio‐imaging unit at Newcastle University is gratefully acknowledged.

Publisher Copyright:
© 2023 The Authors. Advanced Science published by Wiley-VCH GmbH.

Keywords

extracellular exopolysaccharides
packing fraction
biofilms
viscoelasticity
Payne effect

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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title = "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 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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AU - Bible, Amber N.

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AU - Chen, Jinju

AU - Jana, Saikat

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N2 - 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.

AB - 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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Microstructural and Rheological Transitions in Bacterial Biofilms

Abstract

Bibliographical note

Keywords

UN SDGs

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