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The native microbiome of the nematode Caenorhabditis elegans: gateway to a new host-microbiome model

BACKGROUND: Host-microbe associations underlie many key processes of host development, immunity, and life history. Yet, none of the current research on the central model species Caenorhabditis elegans considers the worm’s natural microbiome. Instead, almost all laboratories exclusively use the canon...

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Autores principales: Dirksen, Philipp, Marsh, Sarah Arnaud, Braker, Ines, Heitland, Nele, Wagner, Sophia, Nakad, Rania, Mader, Sebastian, Petersen, Carola, Kowallik, Vienna, Rosenstiel, Philip, Félix, Marie-Anne, Schulenburg, Hinrich
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4860760/
https://www.ncbi.nlm.nih.gov/pubmed/27160191
http://dx.doi.org/10.1186/s12915-016-0258-1
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author Dirksen, Philipp
Marsh, Sarah Arnaud
Braker, Ines
Heitland, Nele
Wagner, Sophia
Nakad, Rania
Mader, Sebastian
Petersen, Carola
Kowallik, Vienna
Rosenstiel, Philip
Félix, Marie-Anne
Schulenburg, Hinrich
author_facet Dirksen, Philipp
Marsh, Sarah Arnaud
Braker, Ines
Heitland, Nele
Wagner, Sophia
Nakad, Rania
Mader, Sebastian
Petersen, Carola
Kowallik, Vienna
Rosenstiel, Philip
Félix, Marie-Anne
Schulenburg, Hinrich
author_sort Dirksen, Philipp
collection PubMed
description BACKGROUND: Host-microbe associations underlie many key processes of host development, immunity, and life history. Yet, none of the current research on the central model species Caenorhabditis elegans considers the worm’s natural microbiome. Instead, almost all laboratories exclusively use the canonical strain N2 and derived mutants, maintained through routine bleach sterilization in monoxenic cultures with an E. coli strain as food. Here, we characterize for the first time the native microbiome of C. elegans and assess its influence on nematode life history characteristics. RESULTS: Nematodes sampled directly from their native habitats carry a species-rich bacterial community, dominated by Proteobacteria such as Enterobacteriaceae and members of the genera Pseudomonas, Stenotrophomonas, Ochrobactrum, and Sphingomonas. The C. elegans microbiome is distinct from that of the worm’s natural environment and the congeneric species C. remanei. Exposure to a derived experimental microbiome revealed that bacterial composition is influenced by host developmental stage and genotype. These experiments also showed that the microbes enhance host fitness under standard and also stressful conditions (e.g., high temperature and either low or high osmolarity). Taking advantage of the nematode’s transparency, we further demonstrate that several Proteobacteria are able to enter the C. elegans gut and that an Ochrobactrum isolate even seems to be able to persist in the intestines under stressful conditions. Moreover, three Pseudomonas isolates produce an anti-fungal effect in vitro which we show can contribute to the worm’s defense against fungal pathogens in vivo. CONCLUSION: This first systematic analysis of the nematode’s native microbiome reveals a species-rich bacterial community to be associated with C. elegans, which is likely of central importance for our understanding of the worm’s biology. The information acquired and the microbial isolates now available for experimental work establishes C. elegans as a tractable model for the in-depth dissection of host-microbiome interactions. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-016-0258-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-48607602016-05-10 The native microbiome of the nematode Caenorhabditis elegans: gateway to a new host-microbiome model Dirksen, Philipp Marsh, Sarah Arnaud Braker, Ines Heitland, Nele Wagner, Sophia Nakad, Rania Mader, Sebastian Petersen, Carola Kowallik, Vienna Rosenstiel, Philip Félix, Marie-Anne Schulenburg, Hinrich BMC Biol Research Article BACKGROUND: Host-microbe associations underlie many key processes of host development, immunity, and life history. Yet, none of the current research on the central model species Caenorhabditis elegans considers the worm’s natural microbiome. Instead, almost all laboratories exclusively use the canonical strain N2 and derived mutants, maintained through routine bleach sterilization in monoxenic cultures with an E. coli strain as food. Here, we characterize for the first time the native microbiome of C. elegans and assess its influence on nematode life history characteristics. RESULTS: Nematodes sampled directly from their native habitats carry a species-rich bacterial community, dominated by Proteobacteria such as Enterobacteriaceae and members of the genera Pseudomonas, Stenotrophomonas, Ochrobactrum, and Sphingomonas. The C. elegans microbiome is distinct from that of the worm’s natural environment and the congeneric species C. remanei. Exposure to a derived experimental microbiome revealed that bacterial composition is influenced by host developmental stage and genotype. These experiments also showed that the microbes enhance host fitness under standard and also stressful conditions (e.g., high temperature and either low or high osmolarity). Taking advantage of the nematode’s transparency, we further demonstrate that several Proteobacteria are able to enter the C. elegans gut and that an Ochrobactrum isolate even seems to be able to persist in the intestines under stressful conditions. Moreover, three Pseudomonas isolates produce an anti-fungal effect in vitro which we show can contribute to the worm’s defense against fungal pathogens in vivo. CONCLUSION: This first systematic analysis of the nematode’s native microbiome reveals a species-rich bacterial community to be associated with C. elegans, which is likely of central importance for our understanding of the worm’s biology. The information acquired and the microbial isolates now available for experimental work establishes C. elegans as a tractable model for the in-depth dissection of host-microbiome interactions. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12915-016-0258-1) contains supplementary material, which is available to authorized users. BioMed Central 2016-05-09 /pmc/articles/PMC4860760/ /pubmed/27160191 http://dx.doi.org/10.1186/s12915-016-0258-1 Text en © Dirksen et al. 2016 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 Article
Dirksen, Philipp
Marsh, Sarah Arnaud
Braker, Ines
Heitland, Nele
Wagner, Sophia
Nakad, Rania
Mader, Sebastian
Petersen, Carola
Kowallik, Vienna
Rosenstiel, Philip
Félix, Marie-Anne
Schulenburg, Hinrich
The native microbiome of the nematode Caenorhabditis elegans: gateway to a new host-microbiome model
title The native microbiome of the nematode Caenorhabditis elegans: gateway to a new host-microbiome model
title_full The native microbiome of the nematode Caenorhabditis elegans: gateway to a new host-microbiome model
title_fullStr The native microbiome of the nematode Caenorhabditis elegans: gateway to a new host-microbiome model
title_full_unstemmed The native microbiome of the nematode Caenorhabditis elegans: gateway to a new host-microbiome model
title_short The native microbiome of the nematode Caenorhabditis elegans: gateway to a new host-microbiome model
title_sort native microbiome of the nematode caenorhabditis elegans: gateway to a new host-microbiome model
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4860760/
https://www.ncbi.nlm.nih.gov/pubmed/27160191
http://dx.doi.org/10.1186/s12915-016-0258-1
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