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Higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics

The assembly and maintenance of microbial diversity in natural communities, despite the abundance of toxin-based antagonistic interactions, presents major challenges for biological understanding. A common framework for investigating such antagonistic interactions involves cyclic dominance games with...

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Detalles Bibliográficos
Autores principales: Swain, Anshuman, Fussell, Levi, Fagan, William F.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740587/
https://www.ncbi.nlm.nih.gov/pubmed/34969851
http://dx.doi.org/10.1073/pnas.2020956119
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author Swain, Anshuman
Fussell, Levi
Fagan, William F.
author_facet Swain, Anshuman
Fussell, Levi
Fagan, William F.
author_sort Swain, Anshuman
collection PubMed
description The assembly and maintenance of microbial diversity in natural communities, despite the abundance of toxin-based antagonistic interactions, presents major challenges for biological understanding. A common framework for investigating such antagonistic interactions involves cyclic dominance games with pairwise interactions. The incorporation of higher-order interactions in such models permits increased levels of microbial diversity, especially in communities in which antibiotic-producing, sensitive, and resistant strains coexist. However, most such models involve a small number of discrete species, assume a notion of pure cyclic dominance, and focus on low mutation rate regimes, none of which well represent the highly interlinked, quickly evolving, and continuous nature of microbial phenotypic space. Here, we present an alternative vision of spatial dynamics for microbial communities based on antagonistic interactions—one in which a large number of species interact in continuous phenotypic space, are capable of rapid mutation, and engage in both direct and higher-order interactions mediated by production of and resistance to antibiotics. Focusing on toxin production, vulnerability, and inhibition among species, we observe highly divergent patterns of diversity and spatial community dynamics. We find that species interaction constraints (rather than mobility) best predict spatiotemporal disturbance regimes, whereas community formation time, mobility, and mutation size best explain patterns of diversity. We also report an intriguing relationship among community formation time, spatial disturbance regimes, and diversity dynamics. This relationship, which suggests that both higher-order interactions and rapid evolution are critical for the origin and maintenance of microbial diversity, has broad-ranging links to the maintenance of diversity in other systems.
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spelling pubmed-87405872022-06-30 Higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics Swain, Anshuman Fussell, Levi Fagan, William F. Proc Natl Acad Sci U S A Biological Sciences The assembly and maintenance of microbial diversity in natural communities, despite the abundance of toxin-based antagonistic interactions, presents major challenges for biological understanding. A common framework for investigating such antagonistic interactions involves cyclic dominance games with pairwise interactions. The incorporation of higher-order interactions in such models permits increased levels of microbial diversity, especially in communities in which antibiotic-producing, sensitive, and resistant strains coexist. However, most such models involve a small number of discrete species, assume a notion of pure cyclic dominance, and focus on low mutation rate regimes, none of which well represent the highly interlinked, quickly evolving, and continuous nature of microbial phenotypic space. Here, we present an alternative vision of spatial dynamics for microbial communities based on antagonistic interactions—one in which a large number of species interact in continuous phenotypic space, are capable of rapid mutation, and engage in both direct and higher-order interactions mediated by production of and resistance to antibiotics. Focusing on toxin production, vulnerability, and inhibition among species, we observe highly divergent patterns of diversity and spatial community dynamics. We find that species interaction constraints (rather than mobility) best predict spatiotemporal disturbance regimes, whereas community formation time, mobility, and mutation size best explain patterns of diversity. We also report an intriguing relationship among community formation time, spatial disturbance regimes, and diversity dynamics. This relationship, which suggests that both higher-order interactions and rapid evolution are critical for the origin and maintenance of microbial diversity, has broad-ranging links to the maintenance of diversity in other systems. National Academy of Sciences 2021-12-30 2022-01-04 /pmc/articles/PMC8740587/ /pubmed/34969851 http://dx.doi.org/10.1073/pnas.2020956119 Text en Copyright © 2021 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Swain, Anshuman
Fussell, Levi
Fagan, William F.
Higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics
title Higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics
title_full Higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics
title_fullStr Higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics
title_full_unstemmed Higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics
title_short Higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics
title_sort higher-order effects, continuous species interactions, and trait evolution shape microbial spatial dynamics
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740587/
https://www.ncbi.nlm.nih.gov/pubmed/34969851
http://dx.doi.org/10.1073/pnas.2020956119
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