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Nutritional and host environments determine community ecology and keystone species in a synthetic gut bacterial community

A challenging task to understand health and disease-related microbiome signatures is to move beyond descriptive community-level profiling towards disentangling microbial interaction networks. Using a synthetic gut bacterial community, we aimed to study the role of individual members in community ass...

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Autores principales: Weiss, Anna S., Niedermeier, Lisa S., von Strempel, Alexandra, Burrichter, Anna G., Ring, Diana, Meng, Chen, Kleigrewe, Karin, Lincetto, Chiara, Hübner, Johannes, Stecher, Bärbel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10409746/
https://www.ncbi.nlm.nih.gov/pubmed/37553336
http://dx.doi.org/10.1038/s41467-023-40372-0
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author Weiss, Anna S.
Niedermeier, Lisa S.
von Strempel, Alexandra
Burrichter, Anna G.
Ring, Diana
Meng, Chen
Kleigrewe, Karin
Lincetto, Chiara
Hübner, Johannes
Stecher, Bärbel
author_facet Weiss, Anna S.
Niedermeier, Lisa S.
von Strempel, Alexandra
Burrichter, Anna G.
Ring, Diana
Meng, Chen
Kleigrewe, Karin
Lincetto, Chiara
Hübner, Johannes
Stecher, Bärbel
author_sort Weiss, Anna S.
collection PubMed
description A challenging task to understand health and disease-related microbiome signatures is to move beyond descriptive community-level profiling towards disentangling microbial interaction networks. Using a synthetic gut bacterial community, we aimed to study the role of individual members in community assembly, identify putative keystone species and test their influence across different environments. Single-species dropout experiments reveal that bacterial strain relationships strongly vary not only in different regions of the murine gut, but also across several standard culture media. Mechanisms involved in environment-dependent keystone functions in vitro include exclusive access to polysaccharides as well as bacteriocin production. Further, Bacteroides caecimuris and Blautia coccoides are found to play keystone roles in gnotobiotic mice by impacting community composition, the metabolic landscape and inflammatory responses. In summary, the presented study highlights the strong interdependency between bacterial community ecology and the biotic and abiotic environment. These results question the concept of universally valid keystone species in the gastrointestinal ecosystem and underline the context-dependency of both, keystone functions and bacterial interaction networks.
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spelling pubmed-104097462023-08-10 Nutritional and host environments determine community ecology and keystone species in a synthetic gut bacterial community Weiss, Anna S. Niedermeier, Lisa S. von Strempel, Alexandra Burrichter, Anna G. Ring, Diana Meng, Chen Kleigrewe, Karin Lincetto, Chiara Hübner, Johannes Stecher, Bärbel Nat Commun Article A challenging task to understand health and disease-related microbiome signatures is to move beyond descriptive community-level profiling towards disentangling microbial interaction networks. Using a synthetic gut bacterial community, we aimed to study the role of individual members in community assembly, identify putative keystone species and test their influence across different environments. Single-species dropout experiments reveal that bacterial strain relationships strongly vary not only in different regions of the murine gut, but also across several standard culture media. Mechanisms involved in environment-dependent keystone functions in vitro include exclusive access to polysaccharides as well as bacteriocin production. Further, Bacteroides caecimuris and Blautia coccoides are found to play keystone roles in gnotobiotic mice by impacting community composition, the metabolic landscape and inflammatory responses. In summary, the presented study highlights the strong interdependency between bacterial community ecology and the biotic and abiotic environment. These results question the concept of universally valid keystone species in the gastrointestinal ecosystem and underline the context-dependency of both, keystone functions and bacterial interaction networks. Nature Publishing Group UK 2023-08-08 /pmc/articles/PMC10409746/ /pubmed/37553336 http://dx.doi.org/10.1038/s41467-023-40372-0 Text en © The Author(s) 2023 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Weiss, Anna S.
Niedermeier, Lisa S.
von Strempel, Alexandra
Burrichter, Anna G.
Ring, Diana
Meng, Chen
Kleigrewe, Karin
Lincetto, Chiara
Hübner, Johannes
Stecher, Bärbel
Nutritional and host environments determine community ecology and keystone species in a synthetic gut bacterial community
title Nutritional and host environments determine community ecology and keystone species in a synthetic gut bacterial community
title_full Nutritional and host environments determine community ecology and keystone species in a synthetic gut bacterial community
title_fullStr Nutritional and host environments determine community ecology and keystone species in a synthetic gut bacterial community
title_full_unstemmed Nutritional and host environments determine community ecology and keystone species in a synthetic gut bacterial community
title_short Nutritional and host environments determine community ecology and keystone species in a synthetic gut bacterial community
title_sort nutritional and host environments determine community ecology and keystone species in a synthetic gut bacterial community
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10409746/
https://www.ncbi.nlm.nih.gov/pubmed/37553336
http://dx.doi.org/10.1038/s41467-023-40372-0
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