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An off-lattice discrete model to characterise filamentous yeast colony morphology

An off-lattice discrete model to characterise filamentous yeast colony morphology
An off-lattice discrete model to characterise filamentous yeast colony morphology

We combine an off-lattice agent-based mathematical model and experimentation to explore filamentous growth of a yeast colony. Under environmental stress, Saccharomyces cerevisiae yeast cells can transition from a bipolar (sated) to unipolar (pseudohyphal) budding mechanism, where cells elongate and bud end-to-end. This budding asymmetry yields spatially non-uniform growth, where filaments extend away from the colony centre, foraging for food. We use approximate Bayesian computation to quantify how individual cell budding mechanisms give rise to spatial patterns observed in experiments. We apply this method of parameter inference to experimental images of colonies of two strains of S. cerevisiae, in low and high nutrient environments. The colony size at the transition from sated to pseudohyphal growth, and a forking mechanism for pseudohyphal cell proliferation are the key features driving colony morphology. Simulations run with the most likely inferred parameters produce colony morphologies that closely resemble experimental results.

1553-734X
Li, Kai
f6a9f82f-dcfa-4c2f-b9fc-486a58755c19
Green, J. Edward F.
79f22dac-8b72-45d9-8e6a-1b9c93ea8afd
Tronnolone, Hayden
c17ba912-b652-49de-a1cc-7c120ee9a19c
Tam, Alexander K.Y.
4037506d-a50e-4a08-8a92-d2022a387932
Black, Andrew J.
f141d87a-ca48-41d4-bd9f-d9bd21e5a2c1
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
Li, Kai
f6a9f82f-dcfa-4c2f-b9fc-486a58755c19
Green, J. Edward F.
79f22dac-8b72-45d9-8e6a-1b9c93ea8afd
Tronnolone, Hayden
c17ba912-b652-49de-a1cc-7c120ee9a19c
Tam, Alexander K.Y.
4037506d-a50e-4a08-8a92-d2022a387932
Black, Andrew J.
f141d87a-ca48-41d4-bd9f-d9bd21e5a2c1
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

Li, Kai, Green, J. Edward F., Tronnolone, Hayden, Tam, Alexander K.Y., Black, Andrew J., Gardner, Jennifer M., Sundstrom, Joanna F., Jiranek, Vladimir and Binder, Benjamin J. (2024) An off-lattice discrete model to characterise filamentous yeast colony morphology. PLoS Computational Biology, 20 (11), [e1012605]. (doi:10.1371/journal.pcbi.1012605).

Record type: Article

Abstract

We combine an off-lattice agent-based mathematical model and experimentation to explore filamentous growth of a yeast colony. Under environmental stress, Saccharomyces cerevisiae yeast cells can transition from a bipolar (sated) to unipolar (pseudohyphal) budding mechanism, where cells elongate and bud end-to-end. This budding asymmetry yields spatially non-uniform growth, where filaments extend away from the colony centre, foraging for food. We use approximate Bayesian computation to quantify how individual cell budding mechanisms give rise to spatial patterns observed in experiments. We apply this method of parameter inference to experimental images of colonies of two strains of S. cerevisiae, in low and high nutrient environments. The colony size at the transition from sated to pseudohyphal growth, and a forking mechanism for pseudohyphal cell proliferation are the key features driving colony morphology. Simulations run with the most likely inferred parameters produce colony morphologies that closely resemble experimental results.

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Accepted/In Press date: 3 November 2024
Published date: 21 November 2024

Identifiers

Local EPrints ID: 497007
URI: http://eprints.soton.ac.uk/id/eprint/497007
ISSN: 1553-734X
PURE UUID: d0d86833-0abc-4bd3-bf79-919a8f9d0309
ORCID for Vladimir Jiranek: ORCID iD orcid.org/0000-0002-9775-8963

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Date deposited: 09 Jan 2025 18:03
Last modified: 22 Aug 2025 02:39

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Contributors

Author: Kai Li
Author: J. Edward F. Green
Author: Hayden Tronnolone
Author: Alexander K.Y. Tam
Author: Andrew J. Black
Author: Jennifer M. Gardner
Author: Joanna F. Sundstrom
Author: Vladimir Jiranek ORCID iD
Author: Benjamin J. Binder

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