Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis
Abstract Background Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the u...
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| Format: | Article |
| Language: | English |
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BMC
2024-02-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-023-01738-0 |
| _version_ | 1797273803723636736 |
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| author | Gaëlle Toullec Nils Rädecker Claudia Pogoreutz Guilhem Banc-Prandi Stéphane Escrig Christel Genoud Cristina Martin Olmos Jorge Spangenberg Anders Meibom |
| author_facet | Gaëlle Toullec Nils Rädecker Claudia Pogoreutz Guilhem Banc-Prandi Stéphane Escrig Christel Genoud Cristina Martin Olmos Jorge Spangenberg Anders Meibom |
| author_sort | Gaëlle Toullec |
| collection | DOAJ |
| description | Abstract Background Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfish Cassiopea has emerged as a powerful experimental model system. Results We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of the Cassiopea holobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronounced in hospite degradation of algal symbionts, which may be a distinct feature of the heat stress response of Cassiopea. Interestingly, this loss of symbionts by degradation was concealed by body shrinkage of the starving animals, resulting in what could be referred to as “invisible” bleaching. Conclusions Overall, our study highlights the importance of the nutritional status in the heat stress response of the Cassiopea holobiont. Compared with other symbiotic cnidarians, the large mesoglea of Cassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in rapidly warming oceans. Video Abstract |
| first_indexed | 2024-03-07T14:49:27Z |
| format | Article |
| id | doaj.art-4110920862914e0b98ecdcd585cb97b1 |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-03-07T14:49:27Z |
| publishDate | 2024-02-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-4110920862914e0b98ecdcd585cb97b12024-03-05T19:45:23ZengBMCMicrobiome2049-26182024-02-0112111710.1186/s40168-023-01738-0Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosisGaëlle Toullec0Nils Rädecker1Claudia Pogoreutz2Guilhem Banc-Prandi3Stéphane Escrig4Christel Genoud5Cristina Martin Olmos6Jorge Spangenberg7Anders Meibom8Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, École Polytechnique Fédérale de Lausanne (EPFL)Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, École Polytechnique Fédérale de Lausanne (EPFL)Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, École Polytechnique Fédérale de Lausanne (EPFL)Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, École Polytechnique Fédérale de Lausanne (EPFL)Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, École Polytechnique Fédérale de Lausanne (EPFL)Electron Microscopy Facility, University of LausanneLaboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, École Polytechnique Fédérale de Lausanne (EPFL)Institute of Earth Surface Dynamics, University of LausanneLaboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering, École Polytechnique Fédérale de Lausanne (EPFL)Abstract Background Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfish Cassiopea has emerged as a powerful experimental model system. Results We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of the Cassiopea holobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronounced in hospite degradation of algal symbionts, which may be a distinct feature of the heat stress response of Cassiopea. Interestingly, this loss of symbionts by degradation was concealed by body shrinkage of the starving animals, resulting in what could be referred to as “invisible” bleaching. Conclusions Overall, our study highlights the importance of the nutritional status in the heat stress response of the Cassiopea holobiont. Compared with other symbiotic cnidarians, the large mesoglea of Cassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in rapidly warming oceans. Video Abstracthttps://doi.org/10.1186/s40168-023-01738-0Climate changePhotosymbiosisCnidariaSymbiodiniaceaeBleachingMetabolism |
| spellingShingle | Gaëlle Toullec Nils Rädecker Claudia Pogoreutz Guilhem Banc-Prandi Stéphane Escrig Christel Genoud Cristina Martin Olmos Jorge Spangenberg Anders Meibom Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis Microbiome Climate change Photosymbiosis Cnidaria Symbiodiniaceae Bleaching Metabolism |
| title | Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis |
| title_full | Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis |
| title_fullStr | Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis |
| title_full_unstemmed | Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis |
| title_short | Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis |
| title_sort | host starvation and in hospite degradation of algal symbionts shape the heat stress response of the cassiopea symbiodiniaceae symbiosis |
| topic | Climate change Photosymbiosis Cnidaria Symbiodiniaceae Bleaching Metabolism |
| url | https://doi.org/10.1186/s40168-023-01738-0 |
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