Symbiont-Mediated Metabolic Shift in the Sea Anemone Anthopleura elegantissima

Abstract

Coral reefs and their photosynthetic algae form one of the most ecologically and economically impactful symbioses in the animal kingdom. The 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. Symbioses with these microeukaryotes have independently evolved multiple times, and non-coral cnidarians (e.g., sea anemones) serve as a valuable and insightful comparative system 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 by the sea anemone Anthopleura elegantissima, which naturally occurs in symbiosis with the dinoflagellate Breviolum muscatinei (formerly Symbiodinium) or the chlorophyte Elliptochloris marina as well as being aposymbiotic. Here, we assembled a draft genome and used multi-omics to characterise multiple physiological levels of each phenotype. We find that A. elegantissima has symbiont-specific transcriptional and metabolomic signatures, but a similar bacterial community dominated by a single Sphingomonas species that is commonly found in the cnidarian microbiome. Symbiosis with either eukaryotic symbiont resulted in differential gene 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. The ability to culture A. elegantissima with its phylogenetically divergent photosymbionts and perform experimental manipulations makes A. elegantissima another tractable sea anemone system to decode the symbiotic conversations of coral reef ecosystems and aid in wider conservation efforts.