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A three-species synthetic community model whose rapid response to antagonism allows the study of higher-order dynamics and emergent properties in minutes

Microbial communities can be considered complex adaptive systems. Understanding how these systems arise from different components and how the dynamics of microbial interactions allow for species coexistence are fundamental questions in ecology. To address these questions, we built a three-species sy...

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Autores principales: Aguilar-Salinas, Bernardo, Olmedo-Álvarez, Gabriela
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272403/
https://www.ncbi.nlm.nih.gov/pubmed/37333661
http://dx.doi.org/10.3389/fmicb.2023.1057883
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author Aguilar-Salinas, Bernardo
Olmedo-Álvarez, Gabriela
author_facet Aguilar-Salinas, Bernardo
Olmedo-Álvarez, Gabriela
author_sort Aguilar-Salinas, Bernardo
collection PubMed
description Microbial communities can be considered complex adaptive systems. Understanding how these systems arise from different components and how the dynamics of microbial interactions allow for species coexistence are fundamental questions in ecology. To address these questions, we built a three-species synthetic community, called BARS (Bacillota A + S + R). Each species in this community exhibits one of three ecological roles: Antagonistic, Sensitive, or Resistant, assigned in the context of a sediment community. We show that the BARS community reproduces features of complex communities and exhibits higher-order interaction (HOI) dynamics. In paired interactions, the majority of the S species (Sutcliffiella horikoshii 20a) population dies within 5 min when paired with the A species (Bacillus pumilus 145). However, an emergent property appears upon adding the third interactor, as antagonism of species A over S is not observed in the presence of the R species (Bacillus cereus 111). For the paired interaction, within the first 5 min, the surviving population of the S species acquires tolerance to species A, and species A ceases antagonism. This qualitative change reflects endogenous dynamics leading to the expression for tolerance to an antagonistic substance. The stability reached in the triple interaction exhibits a nonlinear response, highly sensitive to the density of the R species. In summary, our HOI model allows the study of the assembly dynamics of a three-species community and evaluating the immediate outcome within a 30 min frame. The BARS has features of a complex system where the paired interactions do not predict the community dynamics. The model is amenable to mechanistic dissection and to modeling how the parts integrate to achieve collective properties.
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spelling pubmed-102724032023-06-17 A three-species synthetic community model whose rapid response to antagonism allows the study of higher-order dynamics and emergent properties in minutes Aguilar-Salinas, Bernardo Olmedo-Álvarez, Gabriela Front Microbiol Microbiology Microbial communities can be considered complex adaptive systems. Understanding how these systems arise from different components and how the dynamics of microbial interactions allow for species coexistence are fundamental questions in ecology. To address these questions, we built a three-species synthetic community, called BARS (Bacillota A + S + R). Each species in this community exhibits one of three ecological roles: Antagonistic, Sensitive, or Resistant, assigned in the context of a sediment community. We show that the BARS community reproduces features of complex communities and exhibits higher-order interaction (HOI) dynamics. In paired interactions, the majority of the S species (Sutcliffiella horikoshii 20a) population dies within 5 min when paired with the A species (Bacillus pumilus 145). However, an emergent property appears upon adding the third interactor, as antagonism of species A over S is not observed in the presence of the R species (Bacillus cereus 111). For the paired interaction, within the first 5 min, the surviving population of the S species acquires tolerance to species A, and species A ceases antagonism. This qualitative change reflects endogenous dynamics leading to the expression for tolerance to an antagonistic substance. The stability reached in the triple interaction exhibits a nonlinear response, highly sensitive to the density of the R species. In summary, our HOI model allows the study of the assembly dynamics of a three-species community and evaluating the immediate outcome within a 30 min frame. The BARS has features of a complex system where the paired interactions do not predict the community dynamics. The model is amenable to mechanistic dissection and to modeling how the parts integrate to achieve collective properties. Frontiers Media S.A. 2023-06-02 /pmc/articles/PMC10272403/ /pubmed/37333661 http://dx.doi.org/10.3389/fmicb.2023.1057883 Text en Copyright © 2023 Aguilar-Salinas and Olmedo-Álvarez. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Aguilar-Salinas, Bernardo
Olmedo-Álvarez, Gabriela
A three-species synthetic community model whose rapid response to antagonism allows the study of higher-order dynamics and emergent properties in minutes
title A three-species synthetic community model whose rapid response to antagonism allows the study of higher-order dynamics and emergent properties in minutes
title_full A three-species synthetic community model whose rapid response to antagonism allows the study of higher-order dynamics and emergent properties in minutes
title_fullStr A three-species synthetic community model whose rapid response to antagonism allows the study of higher-order dynamics and emergent properties in minutes
title_full_unstemmed A three-species synthetic community model whose rapid response to antagonism allows the study of higher-order dynamics and emergent properties in minutes
title_short A three-species synthetic community model whose rapid response to antagonism allows the study of higher-order dynamics and emergent properties in minutes
title_sort three-species synthetic community model whose rapid response to antagonism allows the study of higher-order dynamics and emergent properties in minutes
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272403/
https://www.ncbi.nlm.nih.gov/pubmed/37333661
http://dx.doi.org/10.3389/fmicb.2023.1057883
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