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The functional repertoire contained within the native microbiota of the model nematode Caenorhabditis elegans

The microbiota is generally assumed to have a substantial influence on the biology of multicellular organisms. The exact functional contributions of the microbes are often unclear and cannot be inferred easily from 16S rRNA genotyping, which is commonly used for taxonomic characterization of bacteri...

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Autores principales: Zimmermann, Johannes, Obeng, Nancy, Yang, Wentao, Pees, Barbara, Petersen, Carola, Waschina, Silvio, Kissoyan, Kohar A., Aidley, Jack, Hoeppner, Marc P., Bunk, Boyke, Spröer, Cathrin, Leippe, Matthias, Dierking, Katja, Kaleta, Christoph, Schulenburg, Hinrich
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6908608/
https://www.ncbi.nlm.nih.gov/pubmed/31484996
http://dx.doi.org/10.1038/s41396-019-0504-y
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author Zimmermann, Johannes
Obeng, Nancy
Yang, Wentao
Pees, Barbara
Petersen, Carola
Waschina, Silvio
Kissoyan, Kohar A.
Aidley, Jack
Hoeppner, Marc P.
Bunk, Boyke
Spröer, Cathrin
Leippe, Matthias
Dierking, Katja
Kaleta, Christoph
Schulenburg, Hinrich
author_facet Zimmermann, Johannes
Obeng, Nancy
Yang, Wentao
Pees, Barbara
Petersen, Carola
Waschina, Silvio
Kissoyan, Kohar A.
Aidley, Jack
Hoeppner, Marc P.
Bunk, Boyke
Spröer, Cathrin
Leippe, Matthias
Dierking, Katja
Kaleta, Christoph
Schulenburg, Hinrich
author_sort Zimmermann, Johannes
collection PubMed
description The microbiota is generally assumed to have a substantial influence on the biology of multicellular organisms. The exact functional contributions of the microbes are often unclear and cannot be inferred easily from 16S rRNA genotyping, which is commonly used for taxonomic characterization of bacterial associates. In order to bridge this knowledge gap, we here analyzed the metabolic competences of the native microbiota of the model nematode Caenorhabditis elegans. We integrated whole-genome sequences of 77 bacterial microbiota members with metabolic modeling and experimental characterization of bacterial physiology. We found that, as a community, the microbiota can synthesize all essential nutrients for C. elegans. Both metabolic models and experimental analyses revealed that nutrient context can influence how bacteria interact within the microbiota. We identified key bacterial traits that are likely to influence the microbe’s ability to colonize C. elegans (i.e., the ability of bacteria for pyruvate fermentation to acetoin) and affect nematode fitness (i.e., bacterial competence for hydroxyproline degradation). Considering that the microbiota is usually neglected in C. elegans research, the resource presented here will help our understanding of this nematode’s biology in a more natural context. Our integrative approach moreover provides a novel, general framework to characterize microbiota-mediated functions.
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spelling pubmed-69086082019-12-13 The functional repertoire contained within the native microbiota of the model nematode Caenorhabditis elegans Zimmermann, Johannes Obeng, Nancy Yang, Wentao Pees, Barbara Petersen, Carola Waschina, Silvio Kissoyan, Kohar A. Aidley, Jack Hoeppner, Marc P. Bunk, Boyke Spröer, Cathrin Leippe, Matthias Dierking, Katja Kaleta, Christoph Schulenburg, Hinrich ISME J Article The microbiota is generally assumed to have a substantial influence on the biology of multicellular organisms. The exact functional contributions of the microbes are often unclear and cannot be inferred easily from 16S rRNA genotyping, which is commonly used for taxonomic characterization of bacterial associates. In order to bridge this knowledge gap, we here analyzed the metabolic competences of the native microbiota of the model nematode Caenorhabditis elegans. We integrated whole-genome sequences of 77 bacterial microbiota members with metabolic modeling and experimental characterization of bacterial physiology. We found that, as a community, the microbiota can synthesize all essential nutrients for C. elegans. Both metabolic models and experimental analyses revealed that nutrient context can influence how bacteria interact within the microbiota. We identified key bacterial traits that are likely to influence the microbe’s ability to colonize C. elegans (i.e., the ability of bacteria for pyruvate fermentation to acetoin) and affect nematode fitness (i.e., bacterial competence for hydroxyproline degradation). Considering that the microbiota is usually neglected in C. elegans research, the resource presented here will help our understanding of this nematode’s biology in a more natural context. Our integrative approach moreover provides a novel, general framework to characterize microbiota-mediated functions. Nature Publishing Group UK 2019-09-04 2020-01 /pmc/articles/PMC6908608/ /pubmed/31484996 http://dx.doi.org/10.1038/s41396-019-0504-y Text en © The Author(s) 2019 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/.
spellingShingle Article
Zimmermann, Johannes
Obeng, Nancy
Yang, Wentao
Pees, Barbara
Petersen, Carola
Waschina, Silvio
Kissoyan, Kohar A.
Aidley, Jack
Hoeppner, Marc P.
Bunk, Boyke
Spröer, Cathrin
Leippe, Matthias
Dierking, Katja
Kaleta, Christoph
Schulenburg, Hinrich
The functional repertoire contained within the native microbiota of the model nematode Caenorhabditis elegans
title The functional repertoire contained within the native microbiota of the model nematode Caenorhabditis elegans
title_full The functional repertoire contained within the native microbiota of the model nematode Caenorhabditis elegans
title_fullStr The functional repertoire contained within the native microbiota of the model nematode Caenorhabditis elegans
title_full_unstemmed The functional repertoire contained within the native microbiota of the model nematode Caenorhabditis elegans
title_short The functional repertoire contained within the native microbiota of the model nematode Caenorhabditis elegans
title_sort functional repertoire contained within the native microbiota of the model nematode caenorhabditis elegans
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6908608/
https://www.ncbi.nlm.nih.gov/pubmed/31484996
http://dx.doi.org/10.1038/s41396-019-0504-y
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