Octadecanoids as emerging lipid mediators in cnidarian-dinoflagellate symbiosis

Oxylipin signaling has been suggested as a potential mechanism for the inter-partner recognition and homeostasis regulation of cnidarian-dinoflagellate symbiosis, which maintains the ecological viability of coral reefs. Here we assessed the effects of symbiosis and symbiont identity on a model cnidarian, the sea anemone Exaiptasia diaphana, using mass spectrometry to quantify octadecanoid oxylipins (i.e., 18-carbon-derived oxygenated fatty acids). A total of 84 octadecanoids were reported, and distinct stereospecificity was observed for the synthesis of R- and S-enantiomers for symbiont-free anemones and free-living cultured dinoflagellate symbionts, respectively. Symbiont-derived 13(S)-hydroxy-octadecatetraenoic acid (13(S)-HOTE) linked to a putative 13(S)-lipoxygenase was translocated to the host anemone with a 32-fold increase, suggesting it as a biomarker of symbiosis and as a potential agonist of host receptors that regulate inflammatory transcription. Only symbiosis with the native symbiont Breviolum minutum decreased the abundance of pro-inflammatory 9(R)-hydroxy-octadecadienoic acid (9(R)-HODE) in the host. In contrast, symbiosis with the non-native symbiont Durusdinium trenchii was marked by higher abundance of autoxidation-derived octadecanoids, corroborating previous evidence for cellular stress in this association. The putative octadecanoid signaling pathways reported here suggest foundational knowledge gaps that can support the bioengineering and selective breeding of more optimal host-symbiont pairings to enhance resilience and survival of coral reefs.