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Competitive lottery-based assembly of selected clades in the human gut microbiome

BACKGROUND: While the composition of the gut microbiome has now been well described by several large-scale studies, models that can account for the range of microbiome compositions that have been observed are still lacking. One model that has been well studied in macro communities and that could be...

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Autores principales: Verster, Adrian J., Borenstein, Elhanan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6195700/
https://www.ncbi.nlm.nih.gov/pubmed/30340536
http://dx.doi.org/10.1186/s40168-018-0571-8
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author Verster, Adrian J.
Borenstein, Elhanan
author_facet Verster, Adrian J.
Borenstein, Elhanan
author_sort Verster, Adrian J.
collection PubMed
description BACKGROUND: While the composition of the gut microbiome has now been well described by several large-scale studies, models that can account for the range of microbiome compositions that have been observed are still lacking. One model that has been well studied in macro communities and that could be useful for understanding microbiome assembly is the competitive lottery model. This model posits that groups of organisms from a regional pool of species are able to colonize the same niche and that the first species to arrive will take over the entire niche, excluding other group members. RESULTS: Here, we examined whether this model also plays a role in the assembly of the human gut microbiome, defining measures to identify groups of organisms whose distribution across samples conforms to the competitive lottery schema. Applying this model to multiple datasets with thousands of human gut microbiome samples, we identified several taxonomic groups that exhibit a lottery-like distribution, including the Akkermansia, Dialister, and Phascolarctobacterium genera. We validated that these groups exhibit lottery-like assembly in multiple independent microbiome datasets confirming that this assembly schema is universal and not cohort specific. Examining the distribution of species from these groups in the gut microbiome of developing infants, we found that the initial lottery winner can be replaced by a different member of the group. We further found that species from lottery-like groups tend to have fewer genes in their genomes, suggesting more specialized species that are less able to engage in niche differentiation. CONCLUSIONS: Combined, our findings highlight the complex and dynamic process through which microbial communities assemble and suggest that different phylogenetic groups may follow different models during this process. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0571-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-61957002018-10-30 Competitive lottery-based assembly of selected clades in the human gut microbiome Verster, Adrian J. Borenstein, Elhanan Microbiome Research BACKGROUND: While the composition of the gut microbiome has now been well described by several large-scale studies, models that can account for the range of microbiome compositions that have been observed are still lacking. One model that has been well studied in macro communities and that could be useful for understanding microbiome assembly is the competitive lottery model. This model posits that groups of organisms from a regional pool of species are able to colonize the same niche and that the first species to arrive will take over the entire niche, excluding other group members. RESULTS: Here, we examined whether this model also plays a role in the assembly of the human gut microbiome, defining measures to identify groups of organisms whose distribution across samples conforms to the competitive lottery schema. Applying this model to multiple datasets with thousands of human gut microbiome samples, we identified several taxonomic groups that exhibit a lottery-like distribution, including the Akkermansia, Dialister, and Phascolarctobacterium genera. We validated that these groups exhibit lottery-like assembly in multiple independent microbiome datasets confirming that this assembly schema is universal and not cohort specific. Examining the distribution of species from these groups in the gut microbiome of developing infants, we found that the initial lottery winner can be replaced by a different member of the group. We further found that species from lottery-like groups tend to have fewer genes in their genomes, suggesting more specialized species that are less able to engage in niche differentiation. CONCLUSIONS: Combined, our findings highlight the complex and dynamic process through which microbial communities assemble and suggest that different phylogenetic groups may follow different models during this process. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0571-8) contains supplementary material, which is available to authorized users. BioMed Central 2018-10-19 /pmc/articles/PMC6195700/ /pubmed/30340536 http://dx.doi.org/10.1186/s40168-018-0571-8 Text en © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Verster, Adrian J.
Borenstein, Elhanan
Competitive lottery-based assembly of selected clades in the human gut microbiome
title Competitive lottery-based assembly of selected clades in the human gut microbiome
title_full Competitive lottery-based assembly of selected clades in the human gut microbiome
title_fullStr Competitive lottery-based assembly of selected clades in the human gut microbiome
title_full_unstemmed Competitive lottery-based assembly of selected clades in the human gut microbiome
title_short Competitive lottery-based assembly of selected clades in the human gut microbiome
title_sort competitive lottery-based assembly of selected clades in the human gut microbiome
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6195700/
https://www.ncbi.nlm.nih.gov/pubmed/30340536
http://dx.doi.org/10.1186/s40168-018-0571-8
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