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Host Traits and Phylogeny Contribute to Shaping Coral-Bacterial Symbioses

The success of tropical scleractinian corals depends on their ability to establish symbioses with microbial partners. Host phylogeny and traits are known to shape the coral microbiome, but to what extent they affect its composition remains unclear. Here, by using 12 coral species representing the co...

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Autores principales: Ricci, Francesco, Tandon, Kshitij, Black, Jay R., Lê Cao, Kim-Anh, Blackall, Linda L., Verbruggen, Heroen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9045482/
https://www.ncbi.nlm.nih.gov/pubmed/35253476
http://dx.doi.org/10.1128/msystems.00044-22
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author Ricci, Francesco
Tandon, Kshitij
Black, Jay R.
Lê Cao, Kim-Anh
Blackall, Linda L.
Verbruggen, Heroen
author_facet Ricci, Francesco
Tandon, Kshitij
Black, Jay R.
Lê Cao, Kim-Anh
Blackall, Linda L.
Verbruggen, Heroen
author_sort Ricci, Francesco
collection PubMed
description The success of tropical scleractinian corals depends on their ability to establish symbioses with microbial partners. Host phylogeny and traits are known to shape the coral microbiome, but to what extent they affect its composition remains unclear. Here, by using 12 coral species representing the complex and robust clades, we explored the influence of host phylogeny, skeletal architecture, and reproductive mode on the microbiome composition, and further investigated the structure of the tissue and skeleton bacterial communities. Our results show that host phylogeny and traits explained 14% of the tissue and 13% of the skeletal microbiome composition, providing evidence that these predictors contributed to shaping the holobiont in terms of presence and relative abundance of bacterial symbionts. Based on our data, we conclude that host phylogeny affects the presence of specific microbial lineages, reproductive mode predictably influences the microbiome composition, and skeletal architecture works like a filter that affects bacterial relative abundance. We show that the β-diversity of coral tissue and skeleton microbiomes differed, but we found that a large overlapping fraction of bacterial sequences were recovered from both anatomical compartments, supporting the hypothesis that the skeleton can function as a microbial reservoir. Additionally, our analysis of the microbiome structure shows that 99.6% of tissue and 99.7% of skeletal amplicon sequence variants (ASVs) were not consistently present in at least 30% of the samples, suggesting that the coral tissue and skeleton are dominated by rare bacteria. Together, these results provide novel insights into the processes driving coral-bacterial symbioses, along with an improved understanding of the scleractinian microbiome. IMPORTANCE The rapid decline of coral reefs, driven by climate changes, calls for manipulative interventions such as the use of probiotics, which can assist the resilience of these ecosystems. However, many knowledge gaps still exist in our understanding of coral-bacterial symbioses that need to be addressed before effectively applying interventions like probiotics. Here, by investigating the microbiomes of 12 common coral species we show that the associations with bacterial symbionts, thought to be critical to coral health, were influenced to some extent by host phylogeny, skeletal architecture, reproduction, and anatomical compartments. We therefore propose that fundamental and applied functional exploration of coral-associated microbes will help inform successful reef management measures.
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spelling pubmed-90454822022-04-28 Host Traits and Phylogeny Contribute to Shaping Coral-Bacterial Symbioses Ricci, Francesco Tandon, Kshitij Black, Jay R. Lê Cao, Kim-Anh Blackall, Linda L. Verbruggen, Heroen mSystems Research Article The success of tropical scleractinian corals depends on their ability to establish symbioses with microbial partners. Host phylogeny and traits are known to shape the coral microbiome, but to what extent they affect its composition remains unclear. Here, by using 12 coral species representing the complex and robust clades, we explored the influence of host phylogeny, skeletal architecture, and reproductive mode on the microbiome composition, and further investigated the structure of the tissue and skeleton bacterial communities. Our results show that host phylogeny and traits explained 14% of the tissue and 13% of the skeletal microbiome composition, providing evidence that these predictors contributed to shaping the holobiont in terms of presence and relative abundance of bacterial symbionts. Based on our data, we conclude that host phylogeny affects the presence of specific microbial lineages, reproductive mode predictably influences the microbiome composition, and skeletal architecture works like a filter that affects bacterial relative abundance. We show that the β-diversity of coral tissue and skeleton microbiomes differed, but we found that a large overlapping fraction of bacterial sequences were recovered from both anatomical compartments, supporting the hypothesis that the skeleton can function as a microbial reservoir. Additionally, our analysis of the microbiome structure shows that 99.6% of tissue and 99.7% of skeletal amplicon sequence variants (ASVs) were not consistently present in at least 30% of the samples, suggesting that the coral tissue and skeleton are dominated by rare bacteria. Together, these results provide novel insights into the processes driving coral-bacterial symbioses, along with an improved understanding of the scleractinian microbiome. IMPORTANCE The rapid decline of coral reefs, driven by climate changes, calls for manipulative interventions such as the use of probiotics, which can assist the resilience of these ecosystems. However, many knowledge gaps still exist in our understanding of coral-bacterial symbioses that need to be addressed before effectively applying interventions like probiotics. Here, by investigating the microbiomes of 12 common coral species we show that the associations with bacterial symbionts, thought to be critical to coral health, were influenced to some extent by host phylogeny, skeletal architecture, reproduction, and anatomical compartments. We therefore propose that fundamental and applied functional exploration of coral-associated microbes will help inform successful reef management measures. American Society for Microbiology 2022-03-07 /pmc/articles/PMC9045482/ /pubmed/35253476 http://dx.doi.org/10.1128/msystems.00044-22 Text en © Crown copyright 2022. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Ricci, Francesco
Tandon, Kshitij
Black, Jay R.
Lê Cao, Kim-Anh
Blackall, Linda L.
Verbruggen, Heroen
Host Traits and Phylogeny Contribute to Shaping Coral-Bacterial Symbioses
title Host Traits and Phylogeny Contribute to Shaping Coral-Bacterial Symbioses
title_full Host Traits and Phylogeny Contribute to Shaping Coral-Bacterial Symbioses
title_fullStr Host Traits and Phylogeny Contribute to Shaping Coral-Bacterial Symbioses
title_full_unstemmed Host Traits and Phylogeny Contribute to Shaping Coral-Bacterial Symbioses
title_short Host Traits and Phylogeny Contribute to Shaping Coral-Bacterial Symbioses
title_sort host traits and phylogeny contribute to shaping coral-bacterial symbioses
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9045482/
https://www.ncbi.nlm.nih.gov/pubmed/35253476
http://dx.doi.org/10.1128/msystems.00044-22
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