Symbiont Identity Influences Patterns of Symbiosis Establishment, Host Growth, and Asexual Reproduction in a Model Cnidarian-Dinoflagellate Symbiosis.

Abstract

The genus Symbiodinium is physiologically diverse and so may differentially influence symbiosis establishment and function. To explore this, we inoculated aposymbiotic individuals of the sea anemone Exaiptasia pallida (commonly referred to as "Aiptasia"), a model for coral symbiosis, with one of five Symbiodinium species or types (S. microadriaticum, S. minutum, phylotype C3, S. trenchii, or S. voratum). The spatial pattern of colonization was monitored over time via confocal microscopy, and various physiological parameters were measured to assess symbiosis functionality. Anemones rapidly formed a symbiosis with the homologous symbiont, S. minutum, but struggled or failed to form a long-lasting symbiosis with Symbiodinium C3 or S. voratum, respectively. Symbiodinium microadriaticum and S. trenchii were successful but reached their peak density two weeks after S. minutum. The spatial pattern of colonization was identical for all Symbiodinium taxa that were ultimately successful, starting in the oral disk and progressing to the tentacles, before invading the column and, finally, the pedal disk. In all cases, proliferation through the anemone's tentacles was patchy, suggesting that symbionts were being expelled into the gastrovascular cavity and re-phagocytosed by the host. However, the timing of these various spatial events differed between the different Symbiodinium taxa. Furthermore, S. microadriaticum and S. trenchii were less beneficial to the host, as indicated by lower rates of photosynthesis, anemone growth, and pedal laceration. This study enhances our understanding of the link between symbiont identity and the performance of the overall symbiosis, which is important for understanding the potential establishment and persistence of novel host-symbiont pairings. Importantly, we also provide a baseline for further studies on this topic with the globally adopted "Aiptasia" model system.