Amoebocytes facilitate efficient carbon and nitrogen assimilation in the Cassiopea Symbiodiniaceae symbiosis

The upside-down jellyfish Cassiopea engages in symbiosis with
photosynthetic microalgae that facilitate uptake and recycling of
inorganic nutrients. In 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 SEM and 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 assimilation and
translocation of nutrients in Cassiopea, providing an interesting new
model for studies of metabolic interactions in photosymbiotic marine
organisms.