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A multiomic analysis of in situ coral–turf algal interactions

Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associ...

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Autores principales: Roach, Ty N. F., Little, Mark, Arts, Milou G. I., Huckeba, Joel, Haas, Andreas F., George, Emma E., Quinn, Robert A., Cobián-Güemes, Ana G., Naliboff, Douglas S., Silveira, Cynthia B., Vermeij, Mark J. A., Kelly, Linda Wegley, Dorrestein, Pieter C., Rohwer, Forest
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7306781/
https://www.ncbi.nlm.nih.gov/pubmed/32482859
http://dx.doi.org/10.1073/pnas.1915455117
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author Roach, Ty N. F.
Little, Mark
Arts, Milou G. I.
Huckeba, Joel
Haas, Andreas F.
George, Emma E.
Quinn, Robert A.
Cobián-Güemes, Ana G.
Naliboff, Douglas S.
Silveira, Cynthia B.
Vermeij, Mark J. A.
Kelly, Linda Wegley
Dorrestein, Pieter C.
Rohwer, Forest
author_facet Roach, Ty N. F.
Little, Mark
Arts, Milou G. I.
Huckeba, Joel
Haas, Andreas F.
George, Emma E.
Quinn, Robert A.
Cobián-Güemes, Ana G.
Naliboff, Douglas S.
Silveira, Cynthia B.
Vermeij, Mark J. A.
Kelly, Linda Wegley
Dorrestein, Pieter C.
Rohwer, Forest
author_sort Roach, Ty N. F.
collection PubMed
description Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associated metabolites mediate ecological interactions between corals and turf algae. The data demonstrate that there was a microbial assemblage unique to the coral-turf algae interface displaying higher microbial abundances and larger microbial cells. This was consistent with previous studies showing that turf algae exudates feed interface and coral-associated microbial communities, often at the detriment of the coral. Further supporting this hypothesis, when the metabolites were assigned a nominal oxidation state of carbon (NOSC), we found that the turf algal metabolites were significantly more reduced (i.e., have higher potential energy) compared to the corals and interfaces. The algae feeding hypothesis was further supported when the ecological outcomes of interactions (e.g., whether coral was winning or losing) were considered. For example, coral holobionts losing the competition with turf algae had higher Bacteroidetes-to-Firmicutes ratios and an elevated abundance of genes involved in bacterial growth and division. These changes were similar to trends observed in the obese human gut microbiome, where overfeeding of the microbiome creates a dysbiosis detrimental to the long-term health of the metazoan host. Together these results show that there are specific biogeochemical changes at coral–turf algal interfaces that predict the competitive outcomes between holobionts and are consistent with algal exudates feeding coral-associated microbes.
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spelling pubmed-73067812020-06-25 A multiomic analysis of in situ coral–turf algal interactions Roach, Ty N. F. Little, Mark Arts, Milou G. I. Huckeba, Joel Haas, Andreas F. George, Emma E. Quinn, Robert A. Cobián-Güemes, Ana G. Naliboff, Douglas S. Silveira, Cynthia B. Vermeij, Mark J. A. Kelly, Linda Wegley Dorrestein, Pieter C. Rohwer, Forest Proc Natl Acad Sci U S A Biological Sciences Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associated metabolites mediate ecological interactions between corals and turf algae. The data demonstrate that there was a microbial assemblage unique to the coral-turf algae interface displaying higher microbial abundances and larger microbial cells. This was consistent with previous studies showing that turf algae exudates feed interface and coral-associated microbial communities, often at the detriment of the coral. Further supporting this hypothesis, when the metabolites were assigned a nominal oxidation state of carbon (NOSC), we found that the turf algal metabolites were significantly more reduced (i.e., have higher potential energy) compared to the corals and interfaces. The algae feeding hypothesis was further supported when the ecological outcomes of interactions (e.g., whether coral was winning or losing) were considered. For example, coral holobionts losing the competition with turf algae had higher Bacteroidetes-to-Firmicutes ratios and an elevated abundance of genes involved in bacterial growth and division. These changes were similar to trends observed in the obese human gut microbiome, where overfeeding of the microbiome creates a dysbiosis detrimental to the long-term health of the metazoan host. Together these results show that there are specific biogeochemical changes at coral–turf algal interfaces that predict the competitive outcomes between holobionts and are consistent with algal exudates feeding coral-associated microbes. National Academy of Sciences 2020-06-16 2020-06-01 /pmc/articles/PMC7306781/ /pubmed/32482859 http://dx.doi.org/10.1073/pnas.1915455117 Text en Copyright © 2020 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Roach, Ty N. F.
Little, Mark
Arts, Milou G. I.
Huckeba, Joel
Haas, Andreas F.
George, Emma E.
Quinn, Robert A.
Cobián-Güemes, Ana G.
Naliboff, Douglas S.
Silveira, Cynthia B.
Vermeij, Mark J. A.
Kelly, Linda Wegley
Dorrestein, Pieter C.
Rohwer, Forest
A multiomic analysis of in situ coral–turf algal interactions
title A multiomic analysis of in situ coral–turf algal interactions
title_full A multiomic analysis of in situ coral–turf algal interactions
title_fullStr A multiomic analysis of in situ coral–turf algal interactions
title_full_unstemmed A multiomic analysis of in situ coral–turf algal interactions
title_short A multiomic analysis of in situ coral–turf algal interactions
title_sort multiomic analysis of in situ coral–turf algal interactions
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7306781/
https://www.ncbi.nlm.nih.gov/pubmed/32482859
http://dx.doi.org/10.1073/pnas.1915455117
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