Smart utilization of betaine lipids in giant clam Tridacna crocea

Abstract

The giant clam Tridacna crocea inhabits shallow tropical seas with poorly nourished water and severe sun irradiation. They harbor symbiotic algae "zooxanthellae" (dinoflagellate family Symbiodiniaceae) in the mantle tissue and are thought to thrive in this extreme environment by utilizing photosynthetic products from the algae. However, there is no measure of the detailed metabolic flow between the host and symbiont to evaluate one of the most successful symbiotic relationships in nature. Here, we employed liquid chromatography-tandem mass spectrometry (LC-MS/MS)-based lipidomics and Fourier-transform ion cyclotron resonance MS imaging on T. crocea tissues, revealing a unique lipid composition and localization with their symbiont algae. We discovered that the non-phosphorous microalgal betaine lipid diacylglycerylcarboxy-hydroxymethylcholine (DGCC) was present in all tissues and organs of T. crocea to approximately the same degree as phosphatidylcholine (PC). The fatty acid composition of DGCC was similar to that of PC, which is thought to have physiological roles similar to that of DGCC. MS imaging showed co-localization of these lipids throughout the clam tissues. Glycerylcarboxy-hydroxymethylcholine (GCC), the deacylated derivative of DGCC, was found to be a free form of DGCC in the clams and was isolated and characterized from cultured Symbiodiniaceae strains that were isolated from giant clams. These results strongly suggest that giant clams have evolved to smartly utilize DGCCs, phosphorus-free polar lipids of symbiont algae, as essential membrane components to enable them to thrive in oligotrophic coral reef milieu.