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Climate change destabilizes the symbiosis between corals and Symbiodiniaceae. The effects of ocean acidification and warming on critical aspects of coral survical such as symbiotic interactions (i.e., carbon and nitrogen assimilation and exchange) during the planula larval stage remain understudied. By combining physiological and stable isotope techniques, here we show that photosynthesis and carbon and nitrogen assimilation (H 13 CO 3 - and 15 ) in Pocillopora damicornis coral larvae is enhanced under acidification (1000 µatm) and elevated temperature (32 °C). Larvae maintain high survival and settlement rates under these treatment conditions with no observed decline in symbiont densities or signs of bleaching. Acidification and elevated temperature both enhance the net and gross photosynthesis of Symbiodiniaceae. This enhances light respiration and elevates C:N ratios within the holobiont. The increased carbon availability is primarily reflected in the 4 + ) in Pocillopora damicornis coral larvae is enhanced under acidification (1000 µatm) and elevated temperature (32 °C). Larvae maintain high survival and settlement rates under these treatment conditions with no observed decline in symbiont densities or signs of bleaching. Acidification and elevated temperature both enhance the net and gross photosynthesis of Symbiodiniaceae. This enhances light respiration and elevates C:N ratios within the holobiont. The increased carbon availability is primarily reflected in the 13 C enrichment of the host, indicating a greater contribution of the algal symbionts to the host metabolism. We propose that this enhanced mutualistic symbiotic nutrient cycling may bolster coral larvae's resistance to future ocean conditions. This research broadens our understanding of the early life stages of corals by emphasizing the significance of symbiotic interactions beyond those of adult corals., Competing Interests: Competing interests The authors declare no competing interests., (© 2024. The Author(s).)

Objectives: The endosymbiosis with Symbiodiniaceae is key to the ecological success of reef-building corals. However, climate change is threatening to destabilize this symbiosis on a global scale. Most studies looking into the response of corals to heat stress and ocean acidification focus on coral colonies. As such, our knowledge of symbiotic interactions and stress response in other stages of the coral lifecycle remains limited. Establishing transcriptomic resources for coral larvae under stress can thus provide a foundation for understanding the genomic basis of symbiosis, and its susceptibility to climate change. Here, we present a gene expression dataset generated from larvae of the coral Pocillopora damicornis in response to exposure to acidification and elevated temperature conditions below the bleaching threshold of the symbiosis., Data Description: This dataset is comprised of 16 samples (30 larvae per sample) collected from four treatments (Control, High pCO 2 , High Temperature, and Combined pCO 2 and Temperature treatments). Freshly collected larvae were exposed to treatment conditions for five days, providing valuable insights into gene expression in this vulnerable stage of the lifecycle. In combination with previously published datasets, this transcriptomic resource will facilitate the in-depth investigation of the effects of ocean acidification and elevated temperature on coral larvae and its implication for symbiosis., (© 2024. The Author(s).)

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., (© 2024. The Author(s).)

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.IMPORTANCEThe 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., Competing Interests: The authors declare no conflict of interest.