Metabolism of the symbiotic jellyfish Cassiopea in a changing environment

Ocean warming and other anthropogenic impacts have led to a global decline in many photosymbiotic cnidarians, most notably reef-building corals. But some species of the symbiotic and (sub-)tropical upside-down jellyfish Cassiopea are increasingly reported as an expanding and invasive species in coastal regions. Key factors in this ecological success are Cassiopea's trophic plasticity and high heat tolerance. Cassiopea benefit from harboring photosynthetic dinoflagellates (Symbiodiniaceae) that provide organic carbon to the metabolism of their host. Cassiopea medusae are also very effective predators, in part through the release of cassiosomes: submillimeter-scale, autonomous, and motile tissue structures containing abundant stinging cells (nematocytes). Cassiosomes frequently harbor endosymbiotic dinoflagellates and they can kill or paralyze planktonic prey and, as an unpleasant side effect, cause 'contactless' stinging injuries to humans. In contrast to most other photosymbiotic cnidarians, Cassiopea jellyfish exhibit a high tolerance to increasing water temperatures and are rarely observed to bleach in nature. Heat-induced breakdown of algal symbioses has been linked to the destabilization of the nutrient exchange between holobiont partners. However, the effects of heat stress on nutrient cycling within the Cassiopea holobiont remain unknown. This thesis set out to explore the role of symbiotic nutrient cycling in C.andromeda in the context of its high capacity for heterotrophy and tolerance to increasing water temperature. In the first part of this thesis, I investigated the potential contribution of endosymbiotic dinoflagellates to the metabolism and autonomous lifespan of cassiosomes. Stable isotope labeling, correlative SEM-NanoSIMS imaging, and a two-month in vitro survival experiment under either standard light:dark cycling or in total darkness showed that dinoflagellate photosynthesis contributes to cassiosome metabolism and anabolic nitrogen assimilation. Organic carbon input from the dinoflagellates thereby significantly expands the lifespan of cassiosomes and likely enhances the heterotrophic capacity of Cassiopea medusae. In the second part of this thesis, I investigated the impact of acute heat stress on symbiotic nutrient cycling in unfed C. andromeda medusae. Stable isotope labeling, combined with quantitative NanoSIMS imaging, electron microscopy and elemental composition analysis uncovered key processes in the gradual collapse of the Cassiopea holobiont. The medusae heat stress response was driven by host carbon starvation, reduction in the symbiotic supply of photosynthates to the host, and a pronounced in hospite degradation of dinoflagellates. Interestingly, this loss of symbionts was to a large extent concealed by the body shrinkage of the starving animals, resulting in what could be referred to as 'invisible' bleaching.Overall, this work indicates an important role of dinoflagellates in the heterotrophic capacity of Cassiopea by fueling the metabolism and enhancing the lifespan of cassiosomes. It also emphasizes the importance of nutrient cycling and host energy reserves for the thermal tolerance of Cassiopea medusae. The thesis thus contributes to our understanding of general principles underlying heat tolerance in photosymbiotic cnidarians and further strengthens the development of Cassiopea medusae and their cassiosomes as powerful model systems for the study of cnidarian photosymbioses.