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Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa

BACKGROUND: Determining ecological roles of community members and the impact of specific taxa on overall biodiversity in the gastrointestinal (GI) microbiota is of fundamental importance. A step towards a systems-level understanding of the GI microbiota is characterization of biotic interactions. Co...

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Autores principales: Trosvik, Pål, de Muinck, Eric Jacques
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4601151/
https://www.ncbi.nlm.nih.gov/pubmed/26455879
http://dx.doi.org/10.1186/s40168-015-0107-4
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author Trosvik, Pål
de Muinck, Eric Jacques
author_facet Trosvik, Pål
de Muinck, Eric Jacques
author_sort Trosvik, Pål
collection PubMed
description BACKGROUND: Determining ecological roles of community members and the impact of specific taxa on overall biodiversity in the gastrointestinal (GI) microbiota is of fundamental importance. A step towards a systems-level understanding of the GI microbiota is characterization of biotic interactions. Community time series analysis, an approach based on statistical analysis of changing population abundances within a single system over time, is needed in order to say with confidence that one population is affecting the dynamics of another. RESULTS: Here, we characterize biotic interaction structures and define ecological roles of major bacterial groups in four healthy individuals by analysing high-resolution, long-term (>180 days) GI bacterial community time series. Actinobacteria fit the description of a keystone taxon since they are relatively rare, but have a high degree of ecological connectedness, and are positively correlated with diversity both within and between individuals. Bacteriodetes were found to be a foundation taxon in that they are numerically dominant and interact extensively, in particular through positive interactions, with other taxa. Although community structure, diversity and biotic interaction patterns were specific to each individual, we observed a strong tendency towards more intense competition within than between phyla. This is in agreement with Darwin’s limiting similarity hypothesis as well as a published biotic interaction model of the GI microbiota based on reverse ecology. Finally, we link temporal enterotype switching to a reciprocal positive interaction between two key genera. CONCLUSIONS: In this study, we identified ecological roles of key taxa in the human GI microbiota and compared our time series analysis results with those obtained through a reverse ecology approach, providing further evidence in favour of the limiting similarity hypothesis first put forth by Darwin. Larger longitudinal studies are warranted in order to evaluate the generality of basic ecological concepts as applied to the GI microbiota, but our results provide a starting point for achieving a more profound understanding of the GI microbiota as an ecological system. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40168-015-0107-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-46011512015-10-13 Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa Trosvik, Pål de Muinck, Eric Jacques Microbiome Research BACKGROUND: Determining ecological roles of community members and the impact of specific taxa on overall biodiversity in the gastrointestinal (GI) microbiota is of fundamental importance. A step towards a systems-level understanding of the GI microbiota is characterization of biotic interactions. Community time series analysis, an approach based on statistical analysis of changing population abundances within a single system over time, is needed in order to say with confidence that one population is affecting the dynamics of another. RESULTS: Here, we characterize biotic interaction structures and define ecological roles of major bacterial groups in four healthy individuals by analysing high-resolution, long-term (>180 days) GI bacterial community time series. Actinobacteria fit the description of a keystone taxon since they are relatively rare, but have a high degree of ecological connectedness, and are positively correlated with diversity both within and between individuals. Bacteriodetes were found to be a foundation taxon in that they are numerically dominant and interact extensively, in particular through positive interactions, with other taxa. Although community structure, diversity and biotic interaction patterns were specific to each individual, we observed a strong tendency towards more intense competition within than between phyla. This is in agreement with Darwin’s limiting similarity hypothesis as well as a published biotic interaction model of the GI microbiota based on reverse ecology. Finally, we link temporal enterotype switching to a reciprocal positive interaction between two key genera. CONCLUSIONS: In this study, we identified ecological roles of key taxa in the human GI microbiota and compared our time series analysis results with those obtained through a reverse ecology approach, providing further evidence in favour of the limiting similarity hypothesis first put forth by Darwin. Larger longitudinal studies are warranted in order to evaluate the generality of basic ecological concepts as applied to the GI microbiota, but our results provide a starting point for achieving a more profound understanding of the GI microbiota as an ecological system. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s40168-015-0107-4) contains supplementary material, which is available to authorized users. BioMed Central 2015-10-12 /pmc/articles/PMC4601151/ /pubmed/26455879 http://dx.doi.org/10.1186/s40168-015-0107-4 Text en © Trosvik and Muinck. 2015 Open AccessThis 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
Trosvik, Pål
de Muinck, Eric Jacques
Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa
title Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa
title_full Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa
title_fullStr Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa
title_full_unstemmed Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa
title_short Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa
title_sort ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4601151/
https://www.ncbi.nlm.nih.gov/pubmed/26455879
http://dx.doi.org/10.1186/s40168-015-0107-4
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