Oxylipin-mediated metabolic signatures of symbiosis homeostasis and thermal stress in a model sea anemone.

Oxylipins are oxygenated products of fatty acids proposed to exert a regulatory role in cnidarian-dinoflagellate symbiosis; however, this has not been investigated in detail. We integrated physiological measurements and molecular phenotyping with comparative transcriptome mining to examine how the symbiotic cnidarian model, the sea anemone Aiptasia (i.e. Exaiptasia diaphana), and its dinoflagellate symbiont Breviolum minutum respond to symbiosis and thermal stress. We performed lipidomics in combination with the quantification of oxylipins, including octadecanoids, eicosanoids, and docosanoids derived from C18, C20, and C22 fatty acids, respectively, and reconstructed their putative biosynthetic routes through cross-phylogenetic protein sequence homology. Relative to aposymbiotic, symbiotic anemones were enriched with omega-3 fatty acids and downstream octadecanoids of symbiont origin, consistent with inter-partner metabolite flux. Cytochrome P450-derived eicosanoids and docosanoids increased up to 300-fold in symbiotic versus aposymbiotic anemones. Under elevated temperature, anemones showed minor changes in their physiology and lipid profiles; however, the symbiont fraction displayed multiple signatures of stress. In comparison, aposymbiotic anemones showed a 50% reduction in protein abundance as well as structural and storage lipids, while simultaneously accumulating oxylipins linked to inflammation and oxidative stress. Our findings report novel oxylipins that have not been previously observed in dinoflagellates. We identified regulatory pathways that are conserved across cnidarians and higher metazoans, advancing our understanding of cnidarian-dinoflagellate symbiosis and its response to warming climate. We are targeting specific oxylipins and signalling pathways for further research that may aid molecular intervention strategies for selective breeding and assisted evolution to enhance coral resilience in warming oceans.