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Predicting partner fitness based on spatial structuring in a light-driven microbial community

Microbial communities have vital roles in systems essential to human health and agriculture, such as gut and soil microbiomes, and there is growing interest in engineering designer consortia for applications in biotechnology (e.g., personalized probiotics, bioproduction of high-value products, biose...

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Autores principales: Sakkos, Jonathan K., Santos-Merino, María, Kokarakis, Emmanuel J., Li, Bowen, Fuentes-Cabrera, Miguel, Zuliani, Paolo, Ducat, Daniel C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10184905/
https://www.ncbi.nlm.nih.gov/pubmed/37134119
http://dx.doi.org/10.1371/journal.pcbi.1011045
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author Sakkos, Jonathan K.
Santos-Merino, María
Kokarakis, Emmanuel J.
Li, Bowen
Fuentes-Cabrera, Miguel
Zuliani, Paolo
Ducat, Daniel C.
author_facet Sakkos, Jonathan K.
Santos-Merino, María
Kokarakis, Emmanuel J.
Li, Bowen
Fuentes-Cabrera, Miguel
Zuliani, Paolo
Ducat, Daniel C.
author_sort Sakkos, Jonathan K.
collection PubMed
description Microbial communities have vital roles in systems essential to human health and agriculture, such as gut and soil microbiomes, and there is growing interest in engineering designer consortia for applications in biotechnology (e.g., personalized probiotics, bioproduction of high-value products, biosensing). The capacity to monitor and model metabolite exchange in dynamic microbial consortia can provide foundational information important to understand the community level behaviors that emerge, a requirement for building novel consortia. Where experimental approaches for monitoring metabolic exchange are technologically challenging, computational tools can enable greater access to the fate of both chemicals and microbes within a consortium. In this study, we developed an in-silico model of a synthetic microbial consortia of sucrose-secreting Synechococcus elongatus PCC 7942 and Escherichia coli W. Our model was built on the NUFEB framework for Individual-based Modeling (IbM) and optimized for biological accuracy using experimental data. We showed that the relative level of sucrose secretion regulates not only the steady-state support for heterotrophic biomass, but also the temporal dynamics of consortia growth. In order to determine the importance of spatial organization within the consortium, we fit a regression model to spatial data and used it to accurately predict colony fitness. We found that some of the critical parameters for fitness prediction were inter-colony distance, initial biomass, induction level, and distance from the center of the simulation volume. We anticipate that the synergy between experimental and computational approaches will improve our ability to design consortia with novel function.
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spelling pubmed-101849052023-05-16 Predicting partner fitness based on spatial structuring in a light-driven microbial community Sakkos, Jonathan K. Santos-Merino, María Kokarakis, Emmanuel J. Li, Bowen Fuentes-Cabrera, Miguel Zuliani, Paolo Ducat, Daniel C. PLoS Comput Biol Research Article Microbial communities have vital roles in systems essential to human health and agriculture, such as gut and soil microbiomes, and there is growing interest in engineering designer consortia for applications in biotechnology (e.g., personalized probiotics, bioproduction of high-value products, biosensing). The capacity to monitor and model metabolite exchange in dynamic microbial consortia can provide foundational information important to understand the community level behaviors that emerge, a requirement for building novel consortia. Where experimental approaches for monitoring metabolic exchange are technologically challenging, computational tools can enable greater access to the fate of both chemicals and microbes within a consortium. In this study, we developed an in-silico model of a synthetic microbial consortia of sucrose-secreting Synechococcus elongatus PCC 7942 and Escherichia coli W. Our model was built on the NUFEB framework for Individual-based Modeling (IbM) and optimized for biological accuracy using experimental data. We showed that the relative level of sucrose secretion regulates not only the steady-state support for heterotrophic biomass, but also the temporal dynamics of consortia growth. In order to determine the importance of spatial organization within the consortium, we fit a regression model to spatial data and used it to accurately predict colony fitness. We found that some of the critical parameters for fitness prediction were inter-colony distance, initial biomass, induction level, and distance from the center of the simulation volume. We anticipate that the synergy between experimental and computational approaches will improve our ability to design consortia with novel function. Public Library of Science 2023-05-03 /pmc/articles/PMC10184905/ /pubmed/37134119 http://dx.doi.org/10.1371/journal.pcbi.1011045 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 (https://creativecommons.org/publicdomain/zero/1.0/) public domain dedication.
spellingShingle Research Article
Sakkos, Jonathan K.
Santos-Merino, María
Kokarakis, Emmanuel J.
Li, Bowen
Fuentes-Cabrera, Miguel
Zuliani, Paolo
Ducat, Daniel C.
Predicting partner fitness based on spatial structuring in a light-driven microbial community
title Predicting partner fitness based on spatial structuring in a light-driven microbial community
title_full Predicting partner fitness based on spatial structuring in a light-driven microbial community
title_fullStr Predicting partner fitness based on spatial structuring in a light-driven microbial community
title_full_unstemmed Predicting partner fitness based on spatial structuring in a light-driven microbial community
title_short Predicting partner fitness based on spatial structuring in a light-driven microbial community
title_sort predicting partner fitness based on spatial structuring in a light-driven microbial community
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10184905/
https://www.ncbi.nlm.nih.gov/pubmed/37134119
http://dx.doi.org/10.1371/journal.pcbi.1011045
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