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Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata

BACKGROUND: Understanding the associations among corals, their photosynthetic zooxanthella symbionts (Symbiodinium), and coral-associated prokaryotic microbiomes is critical for predicting the fidelity and strength of coral symbioses in the face of growing environmental threats. Most coral-microbiom...

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Autores principales: Sharp, Koty H., Pratte, Zoe A., Kerwin, Allison H., Rotjan, Randi D., Stewart, Frank J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5603060/
https://www.ncbi.nlm.nih.gov/pubmed/28915923
http://dx.doi.org/10.1186/s40168-017-0329-8
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author Sharp, Koty H.
Pratte, Zoe A.
Kerwin, Allison H.
Rotjan, Randi D.
Stewart, Frank J.
author_facet Sharp, Koty H.
Pratte, Zoe A.
Kerwin, Allison H.
Rotjan, Randi D.
Stewart, Frank J.
author_sort Sharp, Koty H.
collection PubMed
description BACKGROUND: Understanding the associations among corals, their photosynthetic zooxanthella symbionts (Symbiodinium), and coral-associated prokaryotic microbiomes is critical for predicting the fidelity and strength of coral symbioses in the face of growing environmental threats. Most coral-microbiome associations are beneficial, yet the mechanisms that determine the composition of the coral microbiome remain largely unknown. Here, we characterized microbiome diversity in the temperate, facultatively symbiotic coral Astrangia poculata at four seasonal time points near the northernmost limit of the species range. The facultative nature of this system allowed us to test seasonal influence and symbiotic state (Symbiodinium density in the coral) on microbiome community composition. RESULTS: Change in season had a strong effect on A. poculata microbiome composition. The seasonal shift was greatest upon the winter to spring transition, during which time A. poculata microbiome composition became more similar among host individuals. Within each of the four seasons, microbiome composition differed significantly from that of surrounding seawater but was surprisingly uniform between symbiotic and aposymbiotic corals, even in summer, when differences in Symbiodinium density between brown and white colonies are the highest, indicating that the observed seasonal shifts are not likely due to fluctuations in Symbiodinium density. CONCLUSIONS: Our results suggest that symbiotic state may not be a primary driver of coral microbial community organization in A. poculata, which is a surprise given the long-held assumption that excess photosynthate is of importance to coral-associated microbes. Rather, other environmental or host factors, in this case, seasonal changes in host physiology associated with winter quiescence, may drive microbiome diversity. Additional studies of A. poculata and other facultatively symbiotic corals will provide important comparisons to studies of reef-building tropical corals and therefore help to identify basic principles of coral microbiome assembly, as well as functional relationships among holobiont members. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-017-0329-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-56030602017-09-20 Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata Sharp, Koty H. Pratte, Zoe A. Kerwin, Allison H. Rotjan, Randi D. Stewart, Frank J. Microbiome Research BACKGROUND: Understanding the associations among corals, their photosynthetic zooxanthella symbionts (Symbiodinium), and coral-associated prokaryotic microbiomes is critical for predicting the fidelity and strength of coral symbioses in the face of growing environmental threats. Most coral-microbiome associations are beneficial, yet the mechanisms that determine the composition of the coral microbiome remain largely unknown. Here, we characterized microbiome diversity in the temperate, facultatively symbiotic coral Astrangia poculata at four seasonal time points near the northernmost limit of the species range. The facultative nature of this system allowed us to test seasonal influence and symbiotic state (Symbiodinium density in the coral) on microbiome community composition. RESULTS: Change in season had a strong effect on A. poculata microbiome composition. The seasonal shift was greatest upon the winter to spring transition, during which time A. poculata microbiome composition became more similar among host individuals. Within each of the four seasons, microbiome composition differed significantly from that of surrounding seawater but was surprisingly uniform between symbiotic and aposymbiotic corals, even in summer, when differences in Symbiodinium density between brown and white colonies are the highest, indicating that the observed seasonal shifts are not likely due to fluctuations in Symbiodinium density. CONCLUSIONS: Our results suggest that symbiotic state may not be a primary driver of coral microbial community organization in A. poculata, which is a surprise given the long-held assumption that excess photosynthate is of importance to coral-associated microbes. Rather, other environmental or host factors, in this case, seasonal changes in host physiology associated with winter quiescence, may drive microbiome diversity. Additional studies of A. poculata and other facultatively symbiotic corals will provide important comparisons to studies of reef-building tropical corals and therefore help to identify basic principles of coral microbiome assembly, as well as functional relationships among holobiont members. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-017-0329-8) contains supplementary material, which is available to authorized users. BioMed Central 2017-09-15 /pmc/articles/PMC5603060/ /pubmed/28915923 http://dx.doi.org/10.1186/s40168-017-0329-8 Text en © The Author(s). 2017 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.
spellingShingle Research
Sharp, Koty H.
Pratte, Zoe A.
Kerwin, Allison H.
Rotjan, Randi D.
Stewart, Frank J.
Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata
title Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata
title_full Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata
title_fullStr Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata
title_full_unstemmed Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata
title_short Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata
title_sort season, but not symbiont state, drives microbiome structure in the temperate coral astrangia poculata
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5603060/
https://www.ncbi.nlm.nih.gov/pubmed/28915923
http://dx.doi.org/10.1186/s40168-017-0329-8
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