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Neutrality in the Metaorganism

Almost all animals and plants are inhabited by diverse communities of microorganisms, the microbiota, thereby forming an integrated entity, the metaorganism. Natural selection should favor hosts that shape the community composition of these microbes to promote a beneficial host-microbe symbiosis. In...

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Autores principales: Sieber, Michael, Pita, Lucía, Weiland-Bräuer, Nancy, Dirksen, Philipp, Wang, Jun, Mortzfeld, Benedikt, Franzenburg, Sören, Schmitz, Ruth A., Baines, John F., Fraune, Sebastian, Hentschel, Ute, Schulenburg, Hinrich, Bosch, Thomas C. G., Traulsen, Arne
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6583948/
https://www.ncbi.nlm.nih.gov/pubmed/31216282
http://dx.doi.org/10.1371/journal.pbio.3000298
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author Sieber, Michael
Pita, Lucía
Weiland-Bräuer, Nancy
Dirksen, Philipp
Wang, Jun
Mortzfeld, Benedikt
Franzenburg, Sören
Schmitz, Ruth A.
Baines, John F.
Fraune, Sebastian
Hentschel, Ute
Schulenburg, Hinrich
Bosch, Thomas C. G.
Traulsen, Arne
author_facet Sieber, Michael
Pita, Lucía
Weiland-Bräuer, Nancy
Dirksen, Philipp
Wang, Jun
Mortzfeld, Benedikt
Franzenburg, Sören
Schmitz, Ruth A.
Baines, John F.
Fraune, Sebastian
Hentschel, Ute
Schulenburg, Hinrich
Bosch, Thomas C. G.
Traulsen, Arne
author_sort Sieber, Michael
collection PubMed
description Almost all animals and plants are inhabited by diverse communities of microorganisms, the microbiota, thereby forming an integrated entity, the metaorganism. Natural selection should favor hosts that shape the community composition of these microbes to promote a beneficial host-microbe symbiosis. Indeed, animal hosts often pose selective environments, which only a subset of the environmentally available microbes are able to colonize. How these microbes assemble after colonization to form the complex microbiota is less clear. Neutral models are based on the assumption that the alternatives in microbiota community composition are selectively equivalent and thus entirely shaped by random population dynamics and dispersal. Here, we use the neutral model as a null hypothesis to assess microbiata composition in host organisms, which does not rely on invoking any adaptive processes underlying microbial community assembly. We show that the overall microbiota community structure from a wide range of host organisms, in particular including previously understudied invertebrates, is in many cases consistent with neutral expectations. Our approach allows to identify individual microbes that are deviating from the neutral expectation and are therefore interesting candidates for further study. Moreover, using simulated communities, we demonstrate that transient community states may play a role in the deviations from the neutral expectation. Our findings highlight that the consideration of neutral processes and temporal changes in community composition are critical for an in-depth understanding of microbiota-host interactions.
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spelling pubmed-65839482019-06-28 Neutrality in the Metaorganism Sieber, Michael Pita, Lucía Weiland-Bräuer, Nancy Dirksen, Philipp Wang, Jun Mortzfeld, Benedikt Franzenburg, Sören Schmitz, Ruth A. Baines, John F. Fraune, Sebastian Hentschel, Ute Schulenburg, Hinrich Bosch, Thomas C. G. Traulsen, Arne PLoS Biol Research Article Almost all animals and plants are inhabited by diverse communities of microorganisms, the microbiota, thereby forming an integrated entity, the metaorganism. Natural selection should favor hosts that shape the community composition of these microbes to promote a beneficial host-microbe symbiosis. Indeed, animal hosts often pose selective environments, which only a subset of the environmentally available microbes are able to colonize. How these microbes assemble after colonization to form the complex microbiota is less clear. Neutral models are based on the assumption that the alternatives in microbiota community composition are selectively equivalent and thus entirely shaped by random population dynamics and dispersal. Here, we use the neutral model as a null hypothesis to assess microbiata composition in host organisms, which does not rely on invoking any adaptive processes underlying microbial community assembly. We show that the overall microbiota community structure from a wide range of host organisms, in particular including previously understudied invertebrates, is in many cases consistent with neutral expectations. Our approach allows to identify individual microbes that are deviating from the neutral expectation and are therefore interesting candidates for further study. Moreover, using simulated communities, we demonstrate that transient community states may play a role in the deviations from the neutral expectation. Our findings highlight that the consideration of neutral processes and temporal changes in community composition are critical for an in-depth understanding of microbiota-host interactions. Public Library of Science 2019-06-19 /pmc/articles/PMC6583948/ /pubmed/31216282 http://dx.doi.org/10.1371/journal.pbio.3000298 Text en © 2019 Sieber et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Sieber, Michael
Pita, Lucía
Weiland-Bräuer, Nancy
Dirksen, Philipp
Wang, Jun
Mortzfeld, Benedikt
Franzenburg, Sören
Schmitz, Ruth A.
Baines, John F.
Fraune, Sebastian
Hentschel, Ute
Schulenburg, Hinrich
Bosch, Thomas C. G.
Traulsen, Arne
Neutrality in the Metaorganism
title Neutrality in the Metaorganism
title_full Neutrality in the Metaorganism
title_fullStr Neutrality in the Metaorganism
title_full_unstemmed Neutrality in the Metaorganism
title_short Neutrality in the Metaorganism
title_sort neutrality in the metaorganism
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6583948/
https://www.ncbi.nlm.nih.gov/pubmed/31216282
http://dx.doi.org/10.1371/journal.pbio.3000298
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