Symbiotic nutrient exchange enhances the long-term survival of cassiosomes, the autonomous stinging-cell structures of Cassiopea

Gaëlle Toullec, Niclas Heidelberg Lyndby, Guilhem Banc-Prandi, Claudia Pogoreutz, Cristina Martin Olmos, Anders Meibom, Nils Rädecker

Research output: Contribution to journalArticlepeer-review

Abstract

Medusae of the widely distributed upside-down jellyfish Cassiopea release autonomous, mobile stinging structures. These so-called cassiosomes play a role in predator defense and prey capture, and are major contributors to “contactless” stinging incidents in (sub-)tropical shallow waters. While the presence of endosymbiotic dinoflagellates in cassiosomes has previously been observed, their potential contribution to the metabolism and long-term survival of cassiosomes is unknown. Combining stable isotope labeling and correlative scanning electron microscopy and nanoscale secondary ion mass spectrometry imaging with a long-term in vitro experiment, our study reveals a mutualistic symbiosis based on nutritional exchanges in dinoflagellate-bearing cassiosomes. We show that organic carbon input from the dinoflagellates fuels the metabolism of the host tissue and enables anabolic nitrogen assimilation. This symbiotic nutrient exchange enhances the life span of cassiosomes for at least one month in vitro. Overall, our study demonstrates that cassiosomes, in analogy with Cassiopea medusae, are photosymbiotic holobionts. Cassiosomes, which are easily accessible under aquarium conditions, promise to be a powerful new miniaturized model system for in-depth ultrastructural and molecular investigation of cnidarian photosymbioses. IMPORTANCE The upside-down jellyfish Cassiopea releases autonomous tissue structures, which are a major cause of contactless stinging incidents in (sub-) tropical coastal waters. These so-called cassiosomes frequently harbor algal symbionts, yet their role in cassiosome functioning and survival is unknown. Our results show that cassiosomes are metabolically active and supported by algal symbionts. Algal photosynthesis enhances the cassiosomes long-term survival in the light. This functional understanding of cassiosomes thereby contributes to explaining the prevalence of contactless stinging incidents and the ecological success of some Cassiopea species. Finally, we show that cassiosomes are miniaturized symbiotic holobionts that can be used to study host-microbe interactions in a simplified system.

Original languageEnglish
JournalmSphere
Volume9
Issue number1
DOIs
StatePublished - 30 Jan 2024
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2024 American Society for Microbiology. All rights reserved.

Funding

We would like to thank C. Genoud, J. Daraspe, and D. De Bellis for their advice on sample preparation and EM observations. A. Daley and her ANOM lab at the University of Lausanne are thanked for sharing their aquarium facility. We thank the editors and two reviewers for their constructive feedback on our manuscript. G.T., G.B.P., A.M., and N.R. were supported by the Swiss National Science Foundation grants 200021_179092 and 212614. C.P. was supported by the Junior Professorship Grant ‘A connected underwater world’ 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 Research (CNRS).

FundersFunder number
French National Centre for Research
Institute of Ecology and the Environment
Agence Nationale de la Recherche
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen ForschungANR-22-CPJ2-0113-01, 212614, 200021_179092
Centre National de la Recherche Scientifique

    Keywords

    • KEYWORDS upside-down jellyfish
    • NanoSIMS
    • Rhizostomae
    • cryo-SEM
    • metabolism
    • photosymbiosis
    • stable isotope labeling

    Fingerprint

    Dive into the research topics of 'Symbiotic nutrient exchange enhances the long-term survival of cassiosomes, the autonomous stinging-cell structures of Cassiopea'. Together they form a unique fingerprint.

    Cite this