A thin-film extensional flow model for biofilm expansion by sliding motility
A thin-film extensional flow model for biofilm expansion by sliding motility
In the presence of glycoproteins, bacterial and yeast biofilms are hypothesized to expand by sliding motility. This involves a sheet of cells spreading as a unit, facilitated by cell proliferation and weak adhesion to the substratum. In this paper, we derive an extensional flow model for biofilm expansion by sliding motility to test this hypothesis. We model the biofilm as a two-phase (living cells and an extracellular matrix) viscous fluid mixture, and model nutrient depletion and uptake from the substratum. Applying the thin-film approximation simplifies the model, and reduces it to one-dimensional axisymmetric form. Comparison with Saccharomyces cerevisiae mat formation experiments reveals good agreement between experimental expansion speed and numerical solutions to the model with O(1) parameters estimated from experiments. This confirms that sliding motility is a possible mechanism for yeast biofilm expansion. Having established the biological relevance of the model, we then demonstrate how the model parameters affect expansion speed, enabling us to predict biofilm expansion for different experimental conditions. Finally, we show that our model can explain the ridge formation observed in some biofilms. This is especially true if surface tension is low, as hypothesized for sliding motility.
Lubrication theory, Mat formation experiments, Multi-phase flow, Saccharomyces cerevisiae, Viscous flow, Yeast
Tam, Alexander
4037506d-a50e-4a08-8a92-d2022a387932
Edward F Green, J.
ef8a01bf-6b18-4b7d-8dda-3c91c283dbb2
Balasuriya, Sanjeeva
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Tek, Ee Lin
7692691a-a6a2-4a7b-964e-235f8ea0ec03
Gardner, Jennifer M.
0d95188b-206d-4817-8437-e163351f6e7f
Sundstrom, Joanna F.
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Jiranek, Vladimir
8e5a8dfd-f5b2-43e3-928b-11dff324abc7
Binder, Benjamin J.
4b861311-8ad2-417c-903a-1d35e541d14b
2019
Tam, Alexander
4037506d-a50e-4a08-8a92-d2022a387932
Edward F Green, J.
ef8a01bf-6b18-4b7d-8dda-3c91c283dbb2
Balasuriya, Sanjeeva
42c5f7a4-ba27-4410-a64e-8a2bfdba19a9
Tek, Ee Lin
7692691a-a6a2-4a7b-964e-235f8ea0ec03
Gardner, Jennifer M.
0d95188b-206d-4817-8437-e163351f6e7f
Sundstrom, Joanna F.
6c6b3452-dfb3-4b5c-aa42-c721eed7b9bb
Jiranek, Vladimir
8e5a8dfd-f5b2-43e3-928b-11dff324abc7
Binder, Benjamin J.
4b861311-8ad2-417c-903a-1d35e541d14b
Tam, Alexander, Edward F Green, J., Balasuriya, Sanjeeva, Tek, Ee Lin, Gardner, Jennifer M., Sundstrom, Joanna F., Jiranek, Vladimir and Binder, Benjamin J.
(2019)
A thin-film extensional flow model for biofilm expansion by sliding motility.
Proceedings of the Royal Society A: Mathematical, Physical and Engineering Sciences, 475 (2229), [20190175].
(doi:10.1098/rspa.2019.0175).
Abstract
In the presence of glycoproteins, bacterial and yeast biofilms are hypothesized to expand by sliding motility. This involves a sheet of cells spreading as a unit, facilitated by cell proliferation and weak adhesion to the substratum. In this paper, we derive an extensional flow model for biofilm expansion by sliding motility to test this hypothesis. We model the biofilm as a two-phase (living cells and an extracellular matrix) viscous fluid mixture, and model nutrient depletion and uptake from the substratum. Applying the thin-film approximation simplifies the model, and reduces it to one-dimensional axisymmetric form. Comparison with Saccharomyces cerevisiae mat formation experiments reveals good agreement between experimental expansion speed and numerical solutions to the model with O(1) parameters estimated from experiments. This confirms that sliding motility is a possible mechanism for yeast biofilm expansion. Having established the biological relevance of the model, we then demonstrate how the model parameters affect expansion speed, enabling us to predict biofilm expansion for different experimental conditions. Finally, we show that our model can explain the ridge formation observed in some biofilms. This is especially true if surface tension is low, as hypothesized for sliding motility.
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Published date: 2019
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Funding Information:
Data accessibility. Data and code for this research are available at The University of Adelaide’s Figshare repository, (https://doi.org/10.25909/5c93294133642), under the Creative Commons CC BY 4.0 license. Competing interests. We declare we have no competing interests. Funding. A.T. received funding from the A. F. Pillow Applied Mathematics Trust, and from the Australian Government under the Research Training Program. J.E.F.G., S.B. and B.J.B. acknowledge funding from the Australian Research Council (ARC), under the grant nos. DE130100031, FT130100484, and DP160102644, respectively. E.L.T. was supported by an Adelaide Graduate Research Scholarship and funding from Wine Australia (GWR Ph1305). J.M.G. and J.F.S. were supported by an ARC grant no. (DP130103547) awarded to V.J. Acknowledgements. The work used supercomputing resources provided by the Phoenix High Performance Computing service at the University of Adelaide.
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© 2019 The Author(s) Published by the Royal Society. All rights reserved.
Keywords:
Lubrication theory, Mat formation experiments, Multi-phase flow, Saccharomyces cerevisiae, Viscous flow, Yeast
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Local EPrints ID: 482663
URI: http://eprints.soton.ac.uk/id/eprint/482663
ISSN: 1364-5021
PURE UUID: a2e494f6-6dea-436e-aa73-ab27de9f1588
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Date deposited: 11 Oct 2023 16:49
Last modified: 18 Mar 2024 04:12
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Contributors
Author:
Alexander Tam
Author:
J. Edward F Green
Author:
Sanjeeva Balasuriya
Author:
Ee Lin Tek
Author:
Jennifer M. Gardner
Author:
Joanna F. Sundstrom
Author:
Vladimir Jiranek
Author:
Benjamin J. Binder
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