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Microbial symbionts and ecological divergence of Caribbean sponges: A new perspective on an ancient association

Marine sponges host diverse communities of microbial symbionts that expand the metabolic capabilities of their host, but the abundance and structure of these communities is highly variable across sponge species. Specificity in these interactions may fuel host niche partitioning on crowded coral reef...

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Autores principales: Freeman, Christopher J., Easson, Cole G., Matterson, Kenan O., Thacker, Robert W., Baker, David M., Paul, Valerie J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7242429/
https://www.ncbi.nlm.nih.gov/pubmed/32203120
http://dx.doi.org/10.1038/s41396-020-0625-3
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author Freeman, Christopher J.
Easson, Cole G.
Matterson, Kenan O.
Thacker, Robert W.
Baker, David M.
Paul, Valerie J.
author_facet Freeman, Christopher J.
Easson, Cole G.
Matterson, Kenan O.
Thacker, Robert W.
Baker, David M.
Paul, Valerie J.
author_sort Freeman, Christopher J.
collection PubMed
description Marine sponges host diverse communities of microbial symbionts that expand the metabolic capabilities of their host, but the abundance and structure of these communities is highly variable across sponge species. Specificity in these interactions may fuel host niche partitioning on crowded coral reefs by allowing individual sponge species to exploit unique sources of carbon and nitrogen, but this hypothesis is yet to be tested. Given the presence of high sponge biomass and the coexistence of diverse sponge species, the Caribbean Sea provides a unique system in which to investigate this hypothesis. To test for ecological divergence among sympatric Caribbean sponges and investigate whether these trends are mediated by microbial symbionts, we measured stable isotope (δ(13)C and δ(15)N) ratios and characterized the microbial community structure of sponge species at sites within four regions spanning a 1700 km latitudinal gradient. There was a low (median of 8.2 %) overlap in the isotopic niches of sympatric species; in addition, host identity accounted for over 75% of the dissimilarity in both δ(13)C and δ(15)N values and microbiome community structure among individual samples within a site. There was also a strong phylogenetic signal in both δ(15)N values and microbial community diversity across host phylogeny, as well as a correlation between microbial community structure and variation in δ(13)C and δ(15)N values across samples. Together, this evidence supports a hypothesis of strong evolutionary selection for ecological divergence across sponge lineages and suggests that this divergence is at least partially mediated by associations with microbial symbionts.
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spelling pubmed-72424292020-05-29 Microbial symbionts and ecological divergence of Caribbean sponges: A new perspective on an ancient association Freeman, Christopher J. Easson, Cole G. Matterson, Kenan O. Thacker, Robert W. Baker, David M. Paul, Valerie J. ISME J Article Marine sponges host diverse communities of microbial symbionts that expand the metabolic capabilities of their host, but the abundance and structure of these communities is highly variable across sponge species. Specificity in these interactions may fuel host niche partitioning on crowded coral reefs by allowing individual sponge species to exploit unique sources of carbon and nitrogen, but this hypothesis is yet to be tested. Given the presence of high sponge biomass and the coexistence of diverse sponge species, the Caribbean Sea provides a unique system in which to investigate this hypothesis. To test for ecological divergence among sympatric Caribbean sponges and investigate whether these trends are mediated by microbial symbionts, we measured stable isotope (δ(13)C and δ(15)N) ratios and characterized the microbial community structure of sponge species at sites within four regions spanning a 1700 km latitudinal gradient. There was a low (median of 8.2 %) overlap in the isotopic niches of sympatric species; in addition, host identity accounted for over 75% of the dissimilarity in both δ(13)C and δ(15)N values and microbiome community structure among individual samples within a site. There was also a strong phylogenetic signal in both δ(15)N values and microbial community diversity across host phylogeny, as well as a correlation between microbial community structure and variation in δ(13)C and δ(15)N values across samples. Together, this evidence supports a hypothesis of strong evolutionary selection for ecological divergence across sponge lineages and suggests that this divergence is at least partially mediated by associations with microbial symbionts. Nature Publishing Group UK 2020-03-20 2020-06 /pmc/articles/PMC7242429/ /pubmed/32203120 http://dx.doi.org/10.1038/s41396-020-0625-3 Text en © The Author(s) 2020 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
Freeman, Christopher J.
Easson, Cole G.
Matterson, Kenan O.
Thacker, Robert W.
Baker, David M.
Paul, Valerie J.
Microbial symbionts and ecological divergence of Caribbean sponges: A new perspective on an ancient association
title Microbial symbionts and ecological divergence of Caribbean sponges: A new perspective on an ancient association
title_full Microbial symbionts and ecological divergence of Caribbean sponges: A new perspective on an ancient association
title_fullStr Microbial symbionts and ecological divergence of Caribbean sponges: A new perspective on an ancient association
title_full_unstemmed Microbial symbionts and ecological divergence of Caribbean sponges: A new perspective on an ancient association
title_short Microbial symbionts and ecological divergence of Caribbean sponges: A new perspective on an ancient association
title_sort microbial symbionts and ecological divergence of caribbean sponges: a new perspective on an ancient association
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7242429/
https://www.ncbi.nlm.nih.gov/pubmed/32203120
http://dx.doi.org/10.1038/s41396-020-0625-3
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