The Cnidarian Bcl-2 Family and Apoptosis: Evidence for Evolutionary Diversity and Involvement in the Onset of Symbiosis

Coral bleaching, which occurs in response to breakdown of cnidarian–dinoflagellate symbiosis, is a major ecological issue that leads to destruction of the entire reef ecosystem. Therefore, understanding the mechanisms regulating symbiosis is of critical importance. One pathway implicated in both establishment and breakdown of cnidarian symbiosis is apoptosis, or programmed cell death. In vertebrates, this process is regulated by the Bcl-2 family, which contains both pro- and antiapoptotic proteins. In corals, Bcl-2 family gene expression is altered during thermal stress, but a role during symbiosis establishment remains unexplored. Additionally, variation in the Bcl-2 repertoire across cnidarians is not well understood. Therefore, we explored the evolution of the Bcl-2 family in cnidarians and their role in regulating apoptosis during symbiosis with homologous and heterologous dinoflagellates using the anemone Exaiptasia diaphana. This was done by correlating apoptosis levels measured by caspase-3 assays with Bcl-2 family gene expression data. The results indicated that each species has a unique repertoire of Bcl-2 proteins, likely as a result of multiple gene loss and duplication events. Functional work revealed that apoptosis was not initiated during recolonization with either homologous or heterologous symbionts, which corresponded to minimal differences in Bcl-2 family gene expression. Additionally, no gene expression changes were observed as a function of steady symbiotic state. Collectively, this work suggests that suppression of apoptosis is a common mechanism used by homologous and heterologous dinoflagellates to form long-term associations with a cnidarian host but members of the Bcl-2 family play a minimal role in this process.