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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Public Library of Science (PLoS)
2021
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oai:doaj.org-article:b5d3e5a515724a449fca718d2c8ac1d02021-12-02T19:57:45ZEmergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia.1553-734X1553-735810.1371/journal.pcbi.1009381https://doaj.org/article/b5d3e5a515724a449fca718d2c8ac1d02021-09-01T00:00:00Zhttps://doi.org/10.1371/journal.pcbi.1009381https://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358The 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.James J WinkleBhargav R KaramchedMatthew R BennettWilliam OttKrešimir JosićPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 17, Iss 9, p e1009381 (2021) |
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Biology (General) QH301-705.5 |
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Biology (General) QH301-705.5 James J Winkle Bhargav R Karamched Matthew R Bennett William Ott Krešimir Josić Emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia. |
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. |
format |
article |
author |
James J Winkle Bhargav R Karamched Matthew R Bennett William Ott Krešimir Josić |
author_facet |
James J Winkle Bhargav R Karamched Matthew R Bennett William Ott Krešimir Josić |
author_sort |
James J Winkle |
title |
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_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_sort |
emergent spatiotemporal population dynamics with cell-length control of synthetic microbial consortia. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2021 |
url |
https://doaj.org/article/b5d3e5a515724a449fca718d2c8ac1d0 |
work_keys_str_mv |
AT jamesjwinkle emergentspatiotemporalpopulationdynamicswithcelllengthcontrolofsyntheticmicrobialconsortia AT bhargavrkaramched emergentspatiotemporalpopulationdynamicswithcelllengthcontrolofsyntheticmicrobialconsortia AT matthewrbennett emergentspatiotemporalpopulationdynamicswithcelllengthcontrolofsyntheticmicrobialconsortia AT williamott emergentspatiotemporalpopulationdynamicswithcelllengthcontrolofsyntheticmicrobialconsortia AT kresimirjosic emergentspatiotemporalpopulationdynamicswithcelllengthcontrolofsyntheticmicrobialconsortia |
_version_ |
1718375798267707392 |