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Peer-reviewedCC BYMolecular ecology

Chilling Injury to Algal Symbionts Induces Host Starvation and Metabolic Reorganization in a Temperate Cnidarian

  1. 1UAR 3278 CRIOBE, PSL Université Paris: EPHE‐UPVD‐CNRS, Université de Perpignan via Domitia
  2. 2University of Plymouth
  3. 3Helmholtz Institute for Functional Marine Biodiversity at the University of Oldenburg

Abstract

Global temperature anomalies increasingly disrupt the cnidarian‐algal symbiosis resulting in a phenomenon termed bleaching. In contrast to heat stress, the mechanisms underlying symbiotic breakdown under cold stress remain largely unknown. Combining physiological and metabolomic measurements, we investigated the response of the photosymbiotic sea anemone holobiont Aiptasia couchii to an experiment mimicking a cold spell in the Mediterranean Sea. Within 4 weeks, we observed the onset of symbiotic breakdown reflected in reduced algal endosymbiont density and chlorophyll a content. While photosynthetic efficiency remained largely unaffected, no gross photosynthesis was detectable in cold‐stressed anemones and decreases in glycosyldiacylglycerols and fatty acyl glycosides indicated chloroplast lipid remobilization. This breakdown of symbiotic carbon cycling was reflected in increased dipeptide and ceramide levels suggesting anemones catabolized protein reserves and induced pre‐apoptotic pathways. Taken together, these responses suggest a decoupling of light and dark reactions of photosynthesis in cold‐stressed endosymbionts, resembling chilling injury in higher plants and free‐living microalgae. This chilling‐induced collapse of symbiotic nutrient cycling eventually leads to host starvation in cold‐stressed Cnidaria. Hence, while cold and heat stress may invoke contrasting physiological effects on endosymbionts, our results suggest that both stressors destabilize the symbiosis through similar mechanisms culminating in host starvation.

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BibTeX
@article{legain2026chilling,
  title = {{Chilling Injury to Algal Symbionts Induces Host Starvation and Metabolic Reorganization in a Temperate Cnidarian}},
  author = {Marie Legain and Taissa Lopes Damasceno and Slimane Chaïb and Miriam Reverter and Héloïse Gauthier and Colin Sten Moldenhauer and Paula Isabel Hueso‐Jiménez and Suzanne C. Mills and Delphine Raviglione and Nils Rädecker and Nathalie Tapissier‐Bontemps and Claudia Pogoreutz},
  journal = {Molecular ecology},
  year = {2026},
  month = oct,
  doi = {10.1111/mec.70582},
  url = {https://europepmc.org/article/PMC/PMC13658927},
  note = {CC BY},
}
RIS
TY  - JOUR
TI  - Chilling Injury to Algal Symbionts Induces Host Starvation and Metabolic Reorganization in a Temperate Cnidarian
AU  - Marie Legain
AU  - Taissa Lopes Damasceno
AU  - Slimane Chaïb
AU  - Miriam Reverter
AU  - Héloïse Gauthier
AU  - Colin Sten Moldenhauer
AU  - Paula Isabel Hueso‐Jiménez
AU  - Suzanne C. Mills
AU  - Delphine Raviglione
AU  - Nils Rädecker
AU  - Nathalie Tapissier‐Bontemps
AU  - Claudia Pogoreutz
PY  - 2026
DA  - 2026/10/01
JO  - Molecular ecology
DO  - 10.1111/mec.70582
UR  - https://europepmc.org/article/PMC/PMC13658927
AB  - Global temperature anomalies increasingly disrupt the cnidarian‐algal symbiosis resulting in a phenomenon termed bleaching. In contrast to heat stress, the mechanisms underlying symbiotic breakdown under cold stress remain largely unknown. Combining physiological and metabolomic measurements, we investigated the response of the photosymbiotic sea anemone holobiont Aiptasia couchii to an experiment mimicking a cold spell in the Mediterranean Sea. Within 4 weeks, we observed the onset of symbiotic breakdown reflected in reduced algal endosymbiont density and chlorophyll a content. While photosynthetic efficiency remained largely unaffected, no gross photosynthesis was detectable in cold‐stressed anemones and decreases in glycosyldiacylglycerols and fatty acyl glycosides indicated chloroplast lipid remobilization. This breakdown of symbiotic carbon cycling was reflected in increased dipeptide and ceramide levels suggesting anemones catabolized protein reserves and induced pre‐apoptotic pathways. Taken together, these responses suggest a decoupling of light and dark reactions of photosynthesis in cold‐stressed endosymbionts, resembling chilling injury in higher plants and free‐living microalgae. This chilling‐induced collapse of symbiotic nutrient cycling eventually leads to host starvation in cold‐stressed Cnidaria. Hence, while cold and heat stress may invoke contrasting physiological effects on endosymbionts, our results suggest that both stressors destabilize the symbiosis through similar mechanisms culminating in host starvation.
SN  - 0962-1083
SN  - 1365-294X
ER  -