Discovery of regulators for early steps of endosymbiosis in the soft coral Xenia

Corals often form a mutually beneficial relationship with the dinoflagellate algae called Symbiodiniaceae. The gastrodermis cells in corals recognize, phagocytose, and house the algae in an organelle called symbiosomes, which support algae photosynthesis and nutrient exchange between corals and algae. Disruptions of this endosymbiotic relationship by environmental stressors cause algae loss, leading to coral bleaching and death, and the degradation of marine ecosystems. Mitigation of coral death requires a mechanistic understanding of coral-algae endosymbiosis. Using a soft coral Xenia species (sp.) as a model, we identified the gene expression patterns of different cell types via single cell RNA-sequencing (scRNA-seq) and uncovered marker genes specifically expressed in endosymbiotic cells4. Here we report the use of RNA interference (RNAi) to establish the function of an endosymbiotic marker gene, Lectin and kazal Protease inhibitor domains (LePin), in mediating endosymbiosis in Xenia. As a secreted lectin, LePin is found on the surface of Xenia mouth tissue. It interacts with free algae and is present in the endosymbiotic cells in the gastrodermis. LePin aids the binding of algae to a region of gastrodermis and supports the formation of new endosymbiotic cells. The evolutionary conservation of LePin among endosymbiotic anthozoans suggests a general role in coral-algae recognition. By coupling bioinformatics analyses with RNAi and scRNA-seq, we further identify two scavenger receptors that support endosymbiosis and may initiate phagocytosis and modulate coral immune response. We also report a requirement of two actin regulators for endosymbiosis, which shed light on the phagocytic machinery and a possible mechanism for symbiosome formation. Our findings should usher in an era of mechanistic studies of coral-alga endosymbiosis.