Symbiont-specific uptake is mediated by integrins in cnidarian larvae

Abstract

The symbiotic relationship between dinoflagellate algae and their cnidarian hosts is fundamental to the health of coral reefs. The selection of appropriate symbionts is paramount for the host to gain valuable nutrients and could be tailored to increase stress tolerance against anthropogenic induced changes in ocean environments, such as coral bleaching in response to ocean warming. Previous research suggests glycan-lectin interactions play a role in symbiont uptake; however, blockage of such interactions does not fully inhibit symbiosis establishment, suggesting other receptors are at play. Potential candidates include RGD peptide binding integrins, which are known to mediate phagocytosis of microbes in other systems. Here, we used a combination of cnidarian model systems and human cell lines to determine if integrins facilitate symbiont recognition and uptake. Integrins are highly expressed in the endodermal tissue of the host, where symbiosis takes place, and upon uptake into endodermal cells, symbionts altered the expression of integrins and downstream signaling molecules. Blockage of integrin binding sites with RGD competitor peptides reduced symbiont uptake, but had no effect on the general uptake of non-symbiotic algae, or uptake in a non-symbiotic cnidarian. In addition, inert beads coated with integrin RGD peptide ligands were phagocytosed more readily than beads coated with scrambled peptide. Finally, overexpression of RGD-binding integrins in human cells increased symbiont uptake and mutation of the active binding site abolished uptake. Our findings reveal RGD-binding integrins as key players in symbiosis establishment and shed light on the evolutionary functions of integrins as phagocytic receptors. Significance statementCorals engage in a symbiotic partnership with photosynthetic algae to survive in challenging environments. To date it is largely unclear how the two partners recognize each other. Using a comparative model systems approach, we have identified evolutionary conserved integrins as molecular receptors for specifically engulfing symbionts, but not other algae. This suggests that integrins allow the host to distinguish between symbiotic and non-symbiotic algae and preferentially take up symbionts. Our findings establish a new paradigm for symbiosis establishment in corals and shed light on the ancient function of integrins as environmental sensors.