Symbiont-mediated metabolic shift in the sea anemone Anthopleura elegantissima

Coral reefs and their photosynthetic algae form one of the most ecologically and economically impactful symbioses in the animal kingdom. Stability of this nutritional mutualism and this ecosystem is, however, at risk due to increasing sea surface temperatures that cause corals to expel their symbionts. Symbiosis with these microeukaryotes has evolved multiple times and non-coral cnidarians (e.g., sea anemones) are insightful comparative systems due to their ease of husbandry in the laboratory and their ability to shuffle different strains of their photosymbionts to acclimate to thermal conditions. This breadth of symbiont shuffling is exemplified in the sea anemone Anthopleura elegantissima, which naturally occurs three symbiotic states: the dinoflagellate Breviolum muscatinei (formally Symbiodinium), the chlorophyte Elliptochloris marina, and aposymbiotic. Here, we use multi-omics to assemble a draft genome as well as characterize multiple physiological levels of each symbiotic state. We find that A. elegantissima has symbiont-state specific transcriptional and metabolomic signatures, but a similar bacterial community dominated by a single Sphingomonus species commonly found in the coral microbiome. Symbiosis with either eukaryotic symbiont resulted in differential expression and metabolic abundance for diverse processes spanning metabolism and immunity to reproduction and development, with some of these processes being unique to either symbiont.