Host starvation and in hospite degradation of algal symbionts shape the heat stress response of the Cassiopea-Symbiodiniaceae symbiosis

Gaëlle Toullec, Nils Rädecker, Claudia Pogoreutz, Guilhem Banc-Prandi, Stéphane Escrig, Christel Genoud, Cristina Martin Olmos, Jorge Spangenberg, Anders Meibom

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

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. 7jQYTVpxtJyVhU5epTFb61 Video Abstract.

Original languageEnglish
Article number42
JournalMicrobiome
Volume12
Issue number1
DOIs
StatePublished - 29 Feb 2024
Externally publishedYes

Bibliographical note

Publisher Copyright:
© The Author(s) 2024.

Funding

GT, NR, GBP, and AM were supported by the Swiss National Science Foundation grants 200021_179092 and 212614. CP was supported by the Junior Professorship Grant number ANR-22-CPJ2-0113–01 awarded by the French National Research Agency and an associated start-up grant by the Institute of Ecology and the Environment (INEE) of the French National Centre for Scientific Research (CNRS). The authors would like to thank N.H. Lyndby for help with the maintenance of the Cassiopea culture tank, K. Vernez for the ammonium measurements of seawater samples, J. Daraspe and D. De Bellis for their advice on sample preparation for EM, and C. Göpfert for the advice on histology. Histological sample preparation was performed with the help of the EPFL Histology Core Facility. The authors would like to thank the editors and two reviewers for their constructive feedback on our manuscript.

FundersFunder number
Institute of Ecology and the Environment
Agence Nationale de la Recherche
École Polytechnique Fédérale de Lausanne
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung212614, 200021_179092, ANR-22-CPJ2-0113–01
Centre National de la Recherche Scientifique

    Keywords

    • Bleaching
    • Climate change
    • Cnidaria
    • Metabolism
    • NanoSIMS
    • Photosymbiosis
    • Symbiodiniaceae

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