The upside-down jellyfish Cassiopea engages in symbiosis with photosynthetic microalgae that facilitate uptake and recycling of inorganic nutrients. By contrast to most other symbiotic cnidarians, algal endosymbionts in Cassiopea are not restricted to the gastroderm but are found in amoebocyte cells within the mesoglea. While symbiont-bearing amoebocytes are highly abundant, their role in nutrient uptake and cycling in Cassiopea remains unknown. By combining isotopic labelling experiments with correlated scanning electron microscopy, and Nano-scale secondary ion mass spectrometry (NanoSIMS) imaging, we quantified the anabolic assimilation of inorganic carbon and nitrogen at the subcellular level in juvenile Cassiopea medusae bell tissue. Amoebocytes were clustered near the sub-umbrella epidermis and facilitated efficient assimilation of inorganic nutrients. Photosynthetically fixed carbon was efficiently translocated between endosymbionts, amoebocytes and host epidermis at rates similar to or exceeding those observed in corals. The Cassiopea holobionts efficiently assimilated ammonium, while no nitrate assimilation was detected, possibly reflecting adaptation to highly dynamic environmental conditions of their natural habitat. The motile amoebocytes allow Cassiopea medusae to distribute their endosymbiont population to optimize access to light and nutrients, and transport nutrition between tissue areas. Amoebocytes thus play a vital role for the assimilation and translocation of nutrients in Cassiopea , providing an interesting new model for studies of metabolic interactions in photosymbiotic marine organisms.

The jellyfishCassiopealargely cover their organic carbon demand via photosynthates produced by their microalgal endosymbionts, but how holobiont morphology and optical properties affect the light microclimate and symbiont photosynthesis inCassiopearemain unexplored. Here, we use optical coherence tomography (OCT) to study the morphology of liveCassiopeamedusae at high spatial resolution. We include detailed 3D reconstructions of external micromorphology, and show the spatial distribution of endosymbionts clustered in amoebocytes and white granules in the bell tissue. Furthermore, we use OCT data to extract inherent optical properties from light scattering white granules inCassiopeaand show that white granules enhance local light availability for symbionts in close proximity. Individual granules had a scattering coefficient of μs= 200-300 cm-1, and a scattering anisotropy factor ofg= 0.7, while large tissue regions filled with white granules had a lower μs= 40-100 cm-1, andg= 0.8-0.9. We combined OCT information with an isotopic labelling experiment to investigate the effect of enhanced light availability in whitish tissue regions. Algal symbionts located in whitish tissue exhibited significantly higher carbon fixation as compared to symbionts in anastomosing tissue (i.e., tissue without light scattering white granules). Our findings support previous suggestions that white granules inCassiopeaplay an important role in the host modulation of the light-microenvironment.