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Causes and consequences of pattern diversification in a spatially self-organizing microbial community

Surface-attached microbial communities constitute a vast amount of life on our planet. They contribute to all major biogeochemical cycles, provide essential services to our society and environment, and have important effects on human health and disease. They typically consist of different interactin...

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Autores principales: Goldschmidt, Felix, Caduff, Lea, Johnson, David R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8319339/
https://www.ncbi.nlm.nih.gov/pubmed/33664433
http://dx.doi.org/10.1038/s41396-021-00942-w
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author Goldschmidt, Felix
Caduff, Lea
Johnson, David R.
author_facet Goldschmidt, Felix
Caduff, Lea
Johnson, David R.
author_sort Goldschmidt, Felix
collection PubMed
description Surface-attached microbial communities constitute a vast amount of life on our planet. They contribute to all major biogeochemical cycles, provide essential services to our society and environment, and have important effects on human health and disease. They typically consist of different interacting genotypes that arrange themselves non-randomly across space (referred to hereafter as spatial self-organization). While spatial self-organization is important for the functioning, ecology, and evolution of these communities, the underlying determinants of spatial self-organization remain unclear. Here, we performed a combination of experiments, statistical modeling, and mathematical simulations with a synthetic cross-feeding microbial community consisting of two isogenic strains. We found that two different patterns of spatial self-organization emerged at the same length and time scales, thus demonstrating pattern diversification. This pattern diversification was not caused by initial environmental heterogeneity or by genetic heterogeneity within populations. Instead, it was caused by nongenetic heterogeneity within populations, and we provide evidence that the source of this nongenetic heterogeneity is local differences in the initial spatial positionings of individuals. We further demonstrate that the different patterns exhibit different community-level properties; namely, they have different expansion speeds. Together, our results demonstrate that pattern diversification can emerge in the absence of initial environmental heterogeneity or genetic heterogeneity within populations and can affect community-level properties, thus providing novel insights into the causes and consequences of microbial spatial self-organization.
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spelling pubmed-83193392021-08-02 Causes and consequences of pattern diversification in a spatially self-organizing microbial community Goldschmidt, Felix Caduff, Lea Johnson, David R. ISME J Article Surface-attached microbial communities constitute a vast amount of life on our planet. They contribute to all major biogeochemical cycles, provide essential services to our society and environment, and have important effects on human health and disease. They typically consist of different interacting genotypes that arrange themselves non-randomly across space (referred to hereafter as spatial self-organization). While spatial self-organization is important for the functioning, ecology, and evolution of these communities, the underlying determinants of spatial self-organization remain unclear. Here, we performed a combination of experiments, statistical modeling, and mathematical simulations with a synthetic cross-feeding microbial community consisting of two isogenic strains. We found that two different patterns of spatial self-organization emerged at the same length and time scales, thus demonstrating pattern diversification. This pattern diversification was not caused by initial environmental heterogeneity or by genetic heterogeneity within populations. Instead, it was caused by nongenetic heterogeneity within populations, and we provide evidence that the source of this nongenetic heterogeneity is local differences in the initial spatial positionings of individuals. We further demonstrate that the different patterns exhibit different community-level properties; namely, they have different expansion speeds. Together, our results demonstrate that pattern diversification can emerge in the absence of initial environmental heterogeneity or genetic heterogeneity within populations and can affect community-level properties, thus providing novel insights into the causes and consequences of microbial spatial self-organization. Nature Publishing Group UK 2021-03-04 2021-08 /pmc/articles/PMC8319339/ /pubmed/33664433 http://dx.doi.org/10.1038/s41396-021-00942-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Goldschmidt, Felix
Caduff, Lea
Johnson, David R.
Causes and consequences of pattern diversification in a spatially self-organizing microbial community
title Causes and consequences of pattern diversification in a spatially self-organizing microbial community
title_full Causes and consequences of pattern diversification in a spatially self-organizing microbial community
title_fullStr Causes and consequences of pattern diversification in a spatially self-organizing microbial community
title_full_unstemmed Causes and consequences of pattern diversification in a spatially self-organizing microbial community
title_short Causes and consequences of pattern diversification in a spatially self-organizing microbial community
title_sort causes and consequences of pattern diversification in a spatially self-organizing microbial community
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8319339/
https://www.ncbi.nlm.nih.gov/pubmed/33664433
http://dx.doi.org/10.1038/s41396-021-00942-w
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