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Species-Specific Viromes in the Ancestral Holobiont Hydra

Recent evidence showing host specificity of colonizing bacteria supports the view that multicellular organisms are holobionts comprised of the macroscopic host in synergistic interdependence with a heterogeneous and host-specific microbial community. Whereas host-bacteria interactions have been exte...

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Autores principales: Grasis, Juris A., Lachnit, Tim, Anton-Erxleben, Friederike, Lim, Yan Wei, Schmieder, Robert, Fraune, Sebastian, Franzenburg, Sören, Insua, Santiago, Machado, GloriaMay, Haynes, Matthew, Little, Mark, Kimble, Robert, Rosenstiel, Philip, Rohwer, Forest L., Bosch, Thomas C. G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4208763/
https://www.ncbi.nlm.nih.gov/pubmed/25343582
http://dx.doi.org/10.1371/journal.pone.0109952
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author Grasis, Juris A.
Lachnit, Tim
Anton-Erxleben, Friederike
Lim, Yan Wei
Schmieder, Robert
Fraune, Sebastian
Franzenburg, Sören
Insua, Santiago
Machado, GloriaMay
Haynes, Matthew
Little, Mark
Kimble, Robert
Rosenstiel, Philip
Rohwer, Forest L.
Bosch, Thomas C. G.
author_facet Grasis, Juris A.
Lachnit, Tim
Anton-Erxleben, Friederike
Lim, Yan Wei
Schmieder, Robert
Fraune, Sebastian
Franzenburg, Sören
Insua, Santiago
Machado, GloriaMay
Haynes, Matthew
Little, Mark
Kimble, Robert
Rosenstiel, Philip
Rohwer, Forest L.
Bosch, Thomas C. G.
author_sort Grasis, Juris A.
collection PubMed
description Recent evidence showing host specificity of colonizing bacteria supports the view that multicellular organisms are holobionts comprised of the macroscopic host in synergistic interdependence with a heterogeneous and host-specific microbial community. Whereas host-bacteria interactions have been extensively investigated, comparatively little is known about host-virus interactions and viral contribution to the holobiont. We sought to determine the viral communities associating with different Hydra species, whether these viral communities were altered with environmental stress, and whether these viruses affect the Hydra-associated holobiont. Here we show that each species of Hydra harbors a diverse host-associated virome. Primary viral families associated with Hydra are Myoviridae, Siphoviridae, Inoviridae, and Herpesviridae. Most Hydra-associated viruses are bacteriophages, a reflection of their involvement in the holobiont. Changes in environmental conditions alter the associated virome, increase viral diversity, and affect the metabolism of the holobiont. The specificity and dynamics of the virome point to potential viral involvement in regulating microbial associations in the Hydra holobiont. While viruses are generally regarded as pathogenic agents, our study suggests an evolutionary conserved ability of viruses to function as holobiont regulators and, therefore, constitutes an emerging paradigm shift in host-microbe interactions.
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spelling pubmed-42087632014-10-27 Species-Specific Viromes in the Ancestral Holobiont Hydra Grasis, Juris A. Lachnit, Tim Anton-Erxleben, Friederike Lim, Yan Wei Schmieder, Robert Fraune, Sebastian Franzenburg, Sören Insua, Santiago Machado, GloriaMay Haynes, Matthew Little, Mark Kimble, Robert Rosenstiel, Philip Rohwer, Forest L. Bosch, Thomas C. G. PLoS One Research Article Recent evidence showing host specificity of colonizing bacteria supports the view that multicellular organisms are holobionts comprised of the macroscopic host in synergistic interdependence with a heterogeneous and host-specific microbial community. Whereas host-bacteria interactions have been extensively investigated, comparatively little is known about host-virus interactions and viral contribution to the holobiont. We sought to determine the viral communities associating with different Hydra species, whether these viral communities were altered with environmental stress, and whether these viruses affect the Hydra-associated holobiont. Here we show that each species of Hydra harbors a diverse host-associated virome. Primary viral families associated with Hydra are Myoviridae, Siphoviridae, Inoviridae, and Herpesviridae. Most Hydra-associated viruses are bacteriophages, a reflection of their involvement in the holobiont. Changes in environmental conditions alter the associated virome, increase viral diversity, and affect the metabolism of the holobiont. The specificity and dynamics of the virome point to potential viral involvement in regulating microbial associations in the Hydra holobiont. While viruses are generally regarded as pathogenic agents, our study suggests an evolutionary conserved ability of viruses to function as holobiont regulators and, therefore, constitutes an emerging paradigm shift in host-microbe interactions. Public Library of Science 2014-10-24 /pmc/articles/PMC4208763/ /pubmed/25343582 http://dx.doi.org/10.1371/journal.pone.0109952 Text en © 2014 Grasis 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, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Grasis, Juris A.
Lachnit, Tim
Anton-Erxleben, Friederike
Lim, Yan Wei
Schmieder, Robert
Fraune, Sebastian
Franzenburg, Sören
Insua, Santiago
Machado, GloriaMay
Haynes, Matthew
Little, Mark
Kimble, Robert
Rosenstiel, Philip
Rohwer, Forest L.
Bosch, Thomas C. G.
Species-Specific Viromes in the Ancestral Holobiont Hydra
title Species-Specific Viromes in the Ancestral Holobiont Hydra
title_full Species-Specific Viromes in the Ancestral Holobiont Hydra
title_fullStr Species-Specific Viromes in the Ancestral Holobiont Hydra
title_full_unstemmed Species-Specific Viromes in the Ancestral Holobiont Hydra
title_short Species-Specific Viromes in the Ancestral Holobiont Hydra
title_sort species-specific viromes in the ancestral holobiont hydra
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4208763/
https://www.ncbi.nlm.nih.gov/pubmed/25343582
http://dx.doi.org/10.1371/journal.pone.0109952
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