Host Traits and Phylogeny Contribute to Shaping Coral-Bacterial Symbioses
ABSTRACT 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 representi...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-04-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00044-22 |
| _version_ | 1818010464037109760 |
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| author | Francesco Ricci Kshitij Tandon Jay R. Black Kim-Anh Lê Cao Linda L. Blackall Heroen Verbruggen |
| author_facet | Francesco Ricci Kshitij Tandon Jay R. Black Kim-Anh Lê Cao Linda L. Blackall Heroen Verbruggen |
| author_sort | Francesco Ricci |
| collection | DOAJ |
| description | ABSTRACT 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. |
| first_indexed | 2024-04-14T05:55:39Z |
| format | Article |
| id | doaj.art-e733ee8808e94e7a878627dc5b418ce8 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-04-14T05:55:39Z |
| publishDate | 2022-04-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-e733ee8808e94e7a878627dc5b418ce82022-12-22T02:08:58ZengAmerican Society for MicrobiologymSystems2379-50772022-04-017210.1128/msystems.00044-22Host Traits and Phylogeny Contribute to Shaping Coral-Bacterial SymbiosesFrancesco Ricci0Kshitij Tandon1Jay R. Black2Kim-Anh Lê Cao3Linda L. Blackall4Heroen Verbruggen5School of BioSciences, University of Melbourne, Victoria, AustraliaSchool of BioSciences, University of Melbourne, Victoria, AustraliaSchool of Geography, Earth and Atmospheric Sciences, University of Melbourne, Victoria, AustraliaMelbourne Integrative Genomics, School of Mathematics and Statistics, University of Melbourne, Victoria, AustraliaSchool of BioSciences, University of Melbourne, Victoria, AustraliaSchool of BioSciences, University of Melbourne, Victoria, AustraliaABSTRACT 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.https://journals.asm.org/doi/10.1128/msystems.00044-22coral microbiomesymbiosisbacteriahost traitsrare microbiomecoral microbiome |
| spellingShingle | Francesco Ricci Kshitij Tandon Jay R. Black Kim-Anh Lê Cao Linda L. Blackall Heroen Verbruggen Host Traits and Phylogeny Contribute to Shaping Coral-Bacterial Symbioses mSystems coral microbiome symbiosis bacteria host traits rare microbiome coral microbiome |
| 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 | coral microbiome symbiosis bacteria host traits rare microbiome coral microbiome |
| url | https://journals.asm.org/doi/10.1128/msystems.00044-22 |
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