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

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          Abstract

          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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          Most cited references 49

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          16S ribosomal DNA amplification for phylogenetic study.

          A set of oligonucleotide primers capable of initiating enzymatic amplification (polymerase chain reaction) on a phylogenetically and taxonomically wide range of bacteria is described along with methods for their use and examples. One pair of primers is capable of amplifying nearly full-length 16S ribosomal DNA (rDNA) from many bacterial genera; the additional primers are useful for various exceptional sequences. Methods for purification of amplified material, direct sequencing, cloning, sequencing, and transcription are outlined. An obligate intracellular parasite of bovine erythrocytes, Anaplasma marginale, is used as an example; its 16S rDNA was amplified, cloned, sequenced, and phylogenetically placed. Anaplasmas are related to the genera Rickettsia and Ehrlichia. In addition, 16S rDNAs from several species were readily amplified from material found in lyophilized ampoules from the American Type Culture Collection. By use of this method, the phylogenetic study of extremely fastidious or highly pathogenic bacterial species can be carried out without the need to culture them. In theory, any gene segment for which polymerase chain reaction primer design is possible can be derived from a readily obtainable lyophilized bacterial culture.
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            An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system.

            The mammalian gastrointestinal tract harbors a complex ecosystem consisting of countless bacteria in homeostasis with the host immune system. Shaped by evolution, this partnership has potential for symbiotic benefit. However, the identities of bacterial molecules mediating symbiosis remain undefined. Here we show that, during colonization of animals with the ubiquitous gut microorganism Bacteroides fragilis, a bacterial polysaccharide (PSA) directs the cellular and physical maturation of the developing immune system. Comparison with germ-free animals reveals that the immunomodulatory activities of PSA during B. fragilis colonization include correcting systemic T cell deficiencies and T(H)1/T(H)2 imbalances and directing lymphoid organogenesis. A PSA mutant of B. fragilis does not restore these immunologic functions. PSA presented by intestinal dendritic cells activates CD4+ T cells and elicits appropriate cytokine production. These findings provide a molecular basis for host-bacterial symbiosis and reveal the archetypal molecule of commensal bacteria that mediates development of the host immune system.
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              “Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics,” in

               T. WHITE,  T Bruns,  S Lee (1990)
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                Author and article information

                Contributors
                hschulenburg@zoologie.uni-kiel.de
                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                9 May 2016
                9 May 2016
                2016
                : 14
                Affiliations
                [ ]Department of Evolutionary Ecology and Genetics, Zoological Institute, Christian-Albrechts University, Am Botanischen Garten 3-9, 24118 Kiel, Germany
                [ ]Institute of Biology of the Ecole Normale Supérieure (IBENS), CNRS, Inserm, 46 rue d’Ulm, 75230 Paris Cedex 05, France
                [ ]Institut Pasteur, 25-28 rue du Docteur Roux, 75724 Paris Cedex 15, France
                [ ]Cologne Excellence Cluster for Cellular Stress Responses in Aging-Associated Diseases, University of Cologne, Joseph-Stelzmann-Str. 26, 50931 Cologne, Germany
                [ ]Max Planck Institute for Evolutionary Biology, August-Thienemann-Strasse 2, 24306 Plön, Germany
                [ ]Institute of Clinical Molecular Biology, Christian-Albrechts University, Am Botanischen Garten 1-3, 24118 Kiel, Germany
                Article
                258
                10.1186/s12915-016-0258-1
                4860760
                27160191
                © 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.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft (DE);
                Award ID: SCHU 1415/11
                Award Recipient :
                Funded by: Bettencourt-Schueller Foundation
                Award ID: Coup d'Elan
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR10-LABX-54 MEMOLIFE
                Funded by: Deutsche Forschungsgemeinschaft (DE)
                Award ID: Project A1 of CRC 1182 Origin and Function of Metaorganisms
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2016

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