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Effects of biofilm heterogeneity on the apparent mechanical properties obtained by shear rheometry

Effects of biofilm heterogeneity on the apparent mechanical properties obtained by shear rheometry
Effects of biofilm heterogeneity on the apparent mechanical properties obtained by shear rheometry

Rheometry is an experimental technique widely used to determine the mechanical properties of biofilms. However, it characterizes the bulk mechanical behavior of the whole biofilm. The effects of biofilm mechanical heterogeneity on rheometry measurements are not known. We used laboratory experiments and computer modeling to explore the effects of biofilm mechanical heterogeneity on the results obtained by rheometry. A synthetic biofilm with layered mechanical properties was studied, and a viscoelastic biofilm theory was employed using the Kelvin–Voigt model. Agar gels with different concentrations were used to prepare the layered, heterogeneous biofilm, which was characterized for mechanical properties in shear mode with a rheometer. Both experiments and simulations indicated that the biofilm properties from rheometry were strongly biased by the weakest portion of the biofilm. The simulation results using linearly stratified mechanical properties from a previous study also showed that the weaker portions of the biofilm dominated the mechanical properties in creep tests. We note that the model can be used as a predictive tool to explore the mechanical behavior of complex biofilm structures beyond those accessible to experiments. Since most biofilms display some degree of mechanical heterogeneity, our results suggest caution should be used in the interpretation of rheometry data. It does not necessarily provide the “average” mechanical properties of the entire biofilm if the mechanical properties are stratified.

Kelvin–Voigt model, biofilm, biofilm modeling, heterogeneous mechanical properties, rheometer
0006-3592
Li, Mengfei
d6ed230a-3c15-4100-8b48-2b575bdd68e5
Nahum, Yanina
fd5b4349-ce26-441e-bdd5-5b3b68a64c86
Matous, Karel
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Stoodley, Paul
08614665-92a9-4466-806e-20c6daeb483f
Nerenberg, Robert
8db640db-2cc5-42e3-8212-83b841005963
Li, Mengfei
d6ed230a-3c15-4100-8b48-2b575bdd68e5
Nahum, Yanina
fd5b4349-ce26-441e-bdd5-5b3b68a64c86
Matous, Karel
c9a6b852-1dd2-45fe-9ec3-ce79df36fb91
Stoodley, Paul
08614665-92a9-4466-806e-20c6daeb483f
Nerenberg, Robert
8db640db-2cc5-42e3-8212-83b841005963

Li, Mengfei, Nahum, Yanina, Matous, Karel, Stoodley, Paul and Nerenberg, Robert (2022) Effects of biofilm heterogeneity on the apparent mechanical properties obtained by shear rheometry. Biotechnology and Bioengineering. (doi:10.1002/bit.28276).

Record type: Article

Abstract

Rheometry is an experimental technique widely used to determine the mechanical properties of biofilms. However, it characterizes the bulk mechanical behavior of the whole biofilm. The effects of biofilm mechanical heterogeneity on rheometry measurements are not known. We used laboratory experiments and computer modeling to explore the effects of biofilm mechanical heterogeneity on the results obtained by rheometry. A synthetic biofilm with layered mechanical properties was studied, and a viscoelastic biofilm theory was employed using the Kelvin–Voigt model. Agar gels with different concentrations were used to prepare the layered, heterogeneous biofilm, which was characterized for mechanical properties in shear mode with a rheometer. Both experiments and simulations indicated that the biofilm properties from rheometry were strongly biased by the weakest portion of the biofilm. The simulation results using linearly stratified mechanical properties from a previous study also showed that the weaker portions of the biofilm dominated the mechanical properties in creep tests. We note that the model can be used as a predictive tool to explore the mechanical behavior of complex biofilm structures beyond those accessible to experiments. Since most biofilms display some degree of mechanical heterogeneity, our results suggest caution should be used in the interpretation of rheometry data. It does not necessarily provide the “average” mechanical properties of the entire biofilm if the mechanical properties are stratified.

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Accepted/In Press date: 24 October 2022
e-pub ahead of print date: 8 November 2022
Additional Information: Funding Information: The rheology tests were performed with instruments at Notre Dame's ND Energy Materials Characterization Facility. The computational resources to run COMSOL Multiphysics were provided by the Notre Dame Center for Research Computing. Partial funding was provided by NSF project #1805406 (RN), the CEST Bayer Fellowship (ML), and the National Institutes of Health project R01GM124436 (PS). Publisher Copyright: © 2022 Wiley Periodicals LLC.
Keywords: Kelvin–Voigt model, biofilm, biofilm modeling, heterogeneous mechanical properties, rheometer

Identifiers

Local EPrints ID: 472205
URI: http://eprints.soton.ac.uk/id/eprint/472205
ISSN: 0006-3592
PURE UUID: d3ea81a9-1fb8-46a6-ae65-c299636617d5
ORCID for Paul Stoodley: ORCID iD orcid.org/0000-0001-6069-273X

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Date deposited: 29 Nov 2022 17:36
Last modified: 17 Mar 2024 07:35

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Contributors

Author: Mengfei Li
Author: Yanina Nahum
Author: Karel Matous
Author: Paul Stoodley ORCID iD
Author: Robert Nerenberg

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