Photobiology and metabolic interactions in the symbiotic jellyfish Cassiopea

The symbiont-bearing jellyfish Cassiopea live a benthic lifestyle, positioning themselves upside-down on sediments in shallow waters to allow their endosymbiotic algae to photosynthesize in the sunlight. Over the last decades Cassiopea has become increasingly popular as a model system for photosymbiosis because, like reef-building corals, these animals rely on autotrophic assimilation of carbon from its algal symbionts. However, relatively little is still known about the photobiology of Cassiopea. Previous studies have focused on investigations of O2 production or CO2 consumption at the scale of entire individuals. Metabolic interactions between animal host and symbiont algae have been studied with bulk isotopic bulk analyses of host tissue vs. the symbiont population. Yet, this symbiosis is the result of single-cell interactions that are modulated by surrounding tissue microenvironments. Accounting for this cellular and spatial heterogeneity of interactions is thus crucial for advancing our understanding of the photobiology of Cassiopea.Unlike reef-building corals, Cassiopea maintain their symbionts in specialized host cells, the motile amoebocytes, residing in the mesoglea of the animal. In the first chapter of this thesis, I thus explored the role of these cells in the nutrient uptake and exchange between host and symbionts. Stable isotope labelling experiments were combined with correlated scanning electron microscopy and NanoSIMS imaging, to achieve a better understanding of the fate of assimilated carbon and the photosynthate translocation in hospite. Amoebocytes hosting clusters of symbionts were found primarily adjacent to the subumbrella epidermis, and incubation experiments with 13C-bicabonate demonstrated that photosynthates produced by the symbiotic algae are transferred via the amoebocytes to host epidermis. Thus, the amoebocytes facilitate nutrient transfer between host and symbionts, and enable host assimilation of autotrophic carbon. Furthermore, incubations with 15NH4+ and 15NO3- demonstrated that Cassiopea prefer NH4+ as their nitrogen source; assimilation of NO3- was not detected in any of the holobiont compartments investigated here by NanoSIMS imaging. Both the symbiotic algae and the host animal contribute to the assimilation of NH4+. In conclusion, the amoebocytes appear to be a key adaptation for the Cassiopea symbiosis, as they facilitate nutrient transfer in hospite and keeps symbionts near the most light-exposed parts of the bell to optimize photosynthesis. In the second chapter, I investigated the photobiology and physico-chemical microenvironment of Cassiopea using microsensors. Photon scalar irradiance across the medusa was found to be highly heterogenous and light availability was found to be highest at the apical parts (i.e., the oral arms and manubrium) of the animal. Surface reflectance revealed that white granules (spheres of ca. 200 µm in diameter) found in the bell tissue along rhopalia canals strongly scatter light, and scalar irradiance measurements showed that light availability was locally enhanced in tissue containing white granules in high density. Depth profiles of O2 concentrations in the bell mesoglea of large individuals (> 6 cm) revealed increasing concentration of O2 down towards the middle of the mesoglea (i.e., halfway between sub- and exumbrella epidermis), in light reaching levels 2-fold higher than the ambient water. During dark periods, the O2 concentration slowly decreased deep