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Emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia

The increased complexity of synthetic microbial biocircuits highlights the need for distributed cell functionality due to concomitant increases in metabolic and regulatory burdens imposed on single-strain topologies. Distributed systems, however, introduce additional challenges since consortium comp...

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Autores principales: Winkle, James J., Karamched, Bhargav R., Bennett, Matthew R., Ott, William, Josić, Krešimir
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8489724/
https://www.ncbi.nlm.nih.gov/pubmed/34550968
http://dx.doi.org/10.1371/journal.pcbi.1009381
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author Winkle, James J.
Karamched, Bhargav R.
Bennett, Matthew R.
Ott, William
Josić, Krešimir
author_facet Winkle, James J.
Karamched, Bhargav R.
Bennett, Matthew R.
Ott, William
Josić, Krešimir
author_sort Winkle, James J.
collection PubMed
description The increased complexity of synthetic microbial biocircuits highlights the need for distributed cell functionality due to concomitant increases in metabolic and regulatory burdens imposed on single-strain topologies. Distributed systems, however, introduce additional challenges since consortium composition and spatiotemporal dynamics of constituent strains must be robustly controlled to achieve desired circuit behaviors. Here, we address these challenges with a modeling-based investigation of emergent spatiotemporal population dynamics using cell-length control in monolayer, two-strain bacterial consortia. We demonstrate that with dynamic control of a strain’s division length, nematic cell alignment in close-packed monolayers can be destabilized. We find that this destabilization confers an emergent, competitive advantage to smaller-length strains—but by mechanisms that differ depending on the spatial patterns of the population. We used complementary modeling approaches to elucidate underlying mechanisms: an agent-based model to simulate detailed mechanical and signaling interactions between the competing strains, and a reductive, stochastic lattice model to represent cell-cell interactions with a single rotational parameter. Our modeling suggests that spatial strain-fraction oscillations can be generated when cell-length control is coupled to quorum-sensing signaling in negative feedback topologies. Our research employs novel methods of population control and points the way to programming strain fraction dynamics in consortial synthetic biology.
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spelling pubmed-84897242021-10-05 Emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia Winkle, James J. Karamched, Bhargav R. Bennett, Matthew R. Ott, William Josić, Krešimir PLoS Comput Biol Research Article The increased complexity of synthetic microbial biocircuits highlights the need for distributed cell functionality due to concomitant increases in metabolic and regulatory burdens imposed on single-strain topologies. Distributed systems, however, introduce additional challenges since consortium composition and spatiotemporal dynamics of constituent strains must be robustly controlled to achieve desired circuit behaviors. Here, we address these challenges with a modeling-based investigation of emergent spatiotemporal population dynamics using cell-length control in monolayer, two-strain bacterial consortia. We demonstrate that with dynamic control of a strain’s division length, nematic cell alignment in close-packed monolayers can be destabilized. We find that this destabilization confers an emergent, competitive advantage to smaller-length strains—but by mechanisms that differ depending on the spatial patterns of the population. We used complementary modeling approaches to elucidate underlying mechanisms: an agent-based model to simulate detailed mechanical and signaling interactions between the competing strains, and a reductive, stochastic lattice model to represent cell-cell interactions with a single rotational parameter. Our modeling suggests that spatial strain-fraction oscillations can be generated when cell-length control is coupled to quorum-sensing signaling in negative feedback topologies. Our research employs novel methods of population control and points the way to programming strain fraction dynamics in consortial synthetic biology. Public Library of Science 2021-09-22 /pmc/articles/PMC8489724/ /pubmed/34550968 http://dx.doi.org/10.1371/journal.pcbi.1009381 Text en © 2021 Winkle et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Winkle, James J.
Karamched, Bhargav R.
Bennett, Matthew R.
Ott, William
Josić, Krešimir
Emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia
title Emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia
title_full Emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia
title_fullStr Emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia
title_full_unstemmed Emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia
title_short Emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia
title_sort emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8489724/
https://www.ncbi.nlm.nih.gov/pubmed/34550968
http://dx.doi.org/10.1371/journal.pcbi.1009381
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