The Influence of Symbiont Identity on the Proteomic and Metabolomic Responses of the Model Cnidarian Aiptasia to Thermal Stress

We examined the effects of symbiont identity and heat stress on the host metabolome and proteome in the cnidarian-dinoflagellate symbiosis. Exaiptasia diaphana ('Aiptasia') was inoculated with its homologous (i.e., native) symbiont Breviolum minutum or a heterologous (i.e., non-native) symbiont (Symbiodinium microadriaticum; Durusdinium trenchii) and thermally stressed. Integrated metabolome and proteome analyses characterised host thermal responses between symbioses, with clear evidence of enhanced nutritional deprivation and cellular stress in hosts harbouring heterologous symbionts following temperature stress. Host metabolomes were partially distinct at the control temperature; however, thermal stress caused metabolomes of anemones containing the two heterologous symbionts to become more alike and more distinct from those containing B. minutum. While these patterns could be partly explained by innate symbiont-specific differences, they may also reflect differences in symbiont density, as under control conditions D. trenchii attained 60% and S. microadriaticum 15% of the density attained by B. minutum, and at elevated temperature only D. trenchii-colonised anemones bleached (60% loss). Our findings add to a growing literature that highlights the physiological limits of partner switching as a means of adaptation to global warming. However, we also provide tentative evidence for improved metabolic functioning with a heterologous symbiont (D. trenchii) after sustained symbiosis.