Symbiodiniaceae Dinoflagellates Express Urease in Three Subcellular Compartments and Upregulate its Expression Levels in situ in Three Organs of a Giant Clam (Tridacna squamosa) During Illumination1

Giant clams harbor three genera of symbiotic dinoflagellates (Symbiodinium,Cladocopium, andDurusdinium) as extracellular symbionts (zooxanthellae). While symbiotic dinoflagellates can synthesize amino acids to benefit the host, they are nitrogen-deficient. Hence, the host must supply them with nitrogen including urea, which can be degraded to ammonia and carbon dioxide by urease (URE). Here, we report three complete coding cDNA sequences ofURE, one for each genus of dinoflagellate, obtained from the colorful outer mantle of the giant clam,Tridacna squamosa. The outer mantle had higher transcript level ofTridacna squamosa zooxanthellae URE(TSZURE) than the whitish inner mantle, foot muscle, hepatopancreas, and ctenidium. TSZURE was immunolocalized strongly and atypically in the plastid, moderately in the cytoplasm, and weakly in the cell wall and plasma membrane of symbiotic dinoflagellates. In the outer mantle, illumination upregulated the protein abundance of TSZURE, which could enhance urea degradation in photosynthesizing dinoflagellates. The urea-nitrogen released could then augment synthesis of amino acids to be shared with the host for its general needs. Illumination also enhanced gene and protein expression levels ofTSZURE/TSZURE in the inner mantle and foot muscle, which contain only small quantities of symbiotic dinoflagellate, have no iridocyte, and lack direct exposure to light. With low phototrophic potential, dinoflagellates in the inner mantle and foot muscle might need to absorb carbohydrates in order to assimilate the urea-nitrogen into amino acids. Amino acids donated by dinoflagellates to the inner mantle and the foot muscle could be used especially for synthesis of organic matrix needed for light-enhanced shell formation and muscle protein, respectively.