Composition of galactolipids, betaine lipids and triglyceride-associated fatty acids of the symbiotic dinoflagellate Zooxanthella (Brandtodinium) nutricula: A glimpse into polyunsaturated fatty acids available to its polycystine radiolarian host

Zooxanthella nutricula is a photosynthetic dinoflagellate symbiont of polycystine radiolarians. As such, it is hypothesized to provide fixed organic carbon, including in the form of acylglycerolipids and sterols, to its non-photosynthetic host. We have previously characterized the sterols of Z. nutricula that may be transferred to its host and, in the present study, have turned our attention to three classes of fatty acid-containing lipids, chloroplast-associated galactolipids, betaine lipids, which are non-phosphorylated phospholipid analogs present in many eukaryotes, and triglycerides. Zooxanthella nutricula was observed using positive-ion electrospray/mass spectrometry (ESI/MS) and ESI/MS/MS to produce the galactolipids mono- and digalactosyldiacylglycerol (MGDG and DGDG, respectively) enriched in octadecapentaenoic (18:5(n-3)) and octadecatetraenoic (18:4(n-3)) acid to place it within a group of peridinin-containing dinoflagellates in a C18/C18 (sn-1/sn-2 fatty acid regiochemistry) cluster, as opposed to another cluster with C20/C18 MGDG and DGDG, where the C20 fatty acid is eicosapentaenoic acid (20:5(n-3)) and the C18 fatty acid is either 18:5(n-3) or 18:4(n-3). Zooxanthella nutricula was also observed to produce 38:10 (total number of fatty acid carbons:total number of double bonds), 38:6, and 44:7 diacylglycerylcarboxyhydroxymethylcholine (DGCC) as the sole type of betaine lipid. Although it is more difficult to determine which fatty acids are present in the sn-1 and sn-2 positions on the glycerol backbone of DGCC using ESI/MS/MS, gas chromatography/mass spectrometry (GC/MS)-based examination indicated the putatively DGCC-associated polyunsaturated fatty acid (PUFA) docosahexaenoic acid (22:6(n-3)). Coupled with the C18 PUFAs of MGDG and DGDG, and fatty acids associated with triglycerides (also examined via GC/MS), Z. nutricula could serve as a rich source of PUFAs for its radiolarian host. These data demonstrate that Z. nutricula produces a similar set of PUFA-containing lipids as Symbiodinium microadriaticum, a photosynthetic dinoflagellate symbiont of cnidarians, indicating a metabolic commonality in these phylogenetically discrete dinoflagellate symbionts with unrelated host organisms.