Destabilization of mutualistic interactions shapes the early heat stress response of the coral holobiont
Abstract Background The stability of the symbiotic relationship between coral and their dinoflagellate algae (Symbiodiniaceae) is disrupted by ocean warming. Although the coral thermal response depends on the complex interactions between host, Symbiodiniaceae and prokaryotes, the mechanisms underlyi...
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BMC
2025-01-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-024-02006-5 |
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| author | Emma Marangon Nils Rädecker Joan Y. Q. Li Marko Terzin Patrick Buerger Nicole S. Webster David G. Bourne Patrick W. Laffy |
| author_facet | Emma Marangon Nils Rädecker Joan Y. Q. Li Marko Terzin Patrick Buerger Nicole S. Webster David G. Bourne Patrick W. Laffy |
| author_sort | Emma Marangon |
| collection | DOAJ |
| description | Abstract Background The stability of the symbiotic relationship between coral and their dinoflagellate algae (Symbiodiniaceae) is disrupted by ocean warming. Although the coral thermal response depends on the complex interactions between host, Symbiodiniaceae and prokaryotes, the mechanisms underlying the initial destabilization of these symbioses are poorly understood. Results In a 2-month manipulative experiment, we exposed the coral Porites lutea to gradually increasing temperatures corresponding to 0–8 degree heating weeks (DHW) and assessed the response of the coral holobiont using coral and Symbiodiniaceae transcriptomics, microbial 16S rRNA gene sequencing and physiological measurements. From early stages of heat stress (< 1 DHW), the increase in metabolic turnover shifted the holobiont to a net heterotrophic state in which algal-derived nutrients were insufficient to meet host energy demands, resulting in reduced holobiont performance at 1 DHW. We postulate the altered nutrient cycling also affected the coral-associated microbial community, with the relative abundance of Endozoicomonas bacteria declining under increasing heat stress. Integration of holobiont stress responses correlated this decline to an increase in expression of a host ADP-ribosylation factor, suggesting that Symbiodiniaceae and Endozoicomonas may underlie similar endosymbiotic regulatory processes. Conclusions The thermotolerance of coral holobionts therefore is influenced by the nutritional status of its members and their interactions, and this identified metabolic interdependency highlights the importance of applying an integrative approach to guide coral reef conservation efforts. Video Abstract |
| format | Article |
| id | doaj-art-39ec8d1a6a374cd186f64663f5b4c7a5 |
| institution | Kabale University |
| issn | 2049-2618 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj-art-39ec8d1a6a374cd186f64663f5b4c7a52025-02-02T12:33:56ZengBMCMicrobiome2049-26182025-01-0113111810.1186/s40168-024-02006-5Destabilization of mutualistic interactions shapes the early heat stress response of the coral holobiontEmma Marangon0Nils Rädecker1Joan Y. Q. Li2Marko Terzin3Patrick Buerger4Nicole S. Webster5David G. Bourne6Patrick W. Laffy7Australian Institute of Marine ScienceLaboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, École Polytechnique Fédérale de LausanneCollege of Science and Engineering, James Cook UniversityAustralian Institute of Marine ScienceApplied Biosciences, Macquarie UniversityAustralian Institute of Marine ScienceAustralian Institute of Marine ScienceAustralian Institute of Marine ScienceAbstract Background The stability of the symbiotic relationship between coral and their dinoflagellate algae (Symbiodiniaceae) is disrupted by ocean warming. Although the coral thermal response depends on the complex interactions between host, Symbiodiniaceae and prokaryotes, the mechanisms underlying the initial destabilization of these symbioses are poorly understood. Results In a 2-month manipulative experiment, we exposed the coral Porites lutea to gradually increasing temperatures corresponding to 0–8 degree heating weeks (DHW) and assessed the response of the coral holobiont using coral and Symbiodiniaceae transcriptomics, microbial 16S rRNA gene sequencing and physiological measurements. From early stages of heat stress (< 1 DHW), the increase in metabolic turnover shifted the holobiont to a net heterotrophic state in which algal-derived nutrients were insufficient to meet host energy demands, resulting in reduced holobiont performance at 1 DHW. We postulate the altered nutrient cycling also affected the coral-associated microbial community, with the relative abundance of Endozoicomonas bacteria declining under increasing heat stress. Integration of holobiont stress responses correlated this decline to an increase in expression of a host ADP-ribosylation factor, suggesting that Symbiodiniaceae and Endozoicomonas may underlie similar endosymbiotic regulatory processes. Conclusions The thermotolerance of coral holobionts therefore is influenced by the nutritional status of its members and their interactions, and this identified metabolic interdependency highlights the importance of applying an integrative approach to guide coral reef conservation efforts. Video Abstracthttps://doi.org/10.1186/s40168-024-02006-5CoralHeat stressSymbiodiniaceaeMicrobiomeGene expression profilingTranscriptomics |
| spellingShingle | Emma Marangon Nils Rädecker Joan Y. Q. Li Marko Terzin Patrick Buerger Nicole S. Webster David G. Bourne Patrick W. Laffy Destabilization of mutualistic interactions shapes the early heat stress response of the coral holobiont Microbiome Coral Heat stress Symbiodiniaceae Microbiome Gene expression profiling Transcriptomics |
| title | Destabilization of mutualistic interactions shapes the early heat stress response of the coral holobiont |
| title_full | Destabilization of mutualistic interactions shapes the early heat stress response of the coral holobiont |
| title_fullStr | Destabilization of mutualistic interactions shapes the early heat stress response of the coral holobiont |
| title_full_unstemmed | Destabilization of mutualistic interactions shapes the early heat stress response of the coral holobiont |
| title_short | Destabilization of mutualistic interactions shapes the early heat stress response of the coral holobiont |
| title_sort | destabilization of mutualistic interactions shapes the early heat stress response of the coral holobiont |
| topic | Coral Heat stress Symbiodiniaceae Microbiome Gene expression profiling Transcriptomics |
| url | https://doi.org/10.1186/s40168-024-02006-5 |
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