Proteomes of native and non-native symbionts reveal responses underpinning host-symbiont specificity in the cnidarian-dinoflagellate symbiosis.

Abstract

Cellular mechanisms responsible for the regulation of nutrient exchange, immune responses, and symbiont population growth in the cnidarian-dinoflagellate symbiosis are poorly resolved, particularly with respect to the dinoflagellate symbiont. Here, we characterised proteomic changes in the native symbiont Breviolum minutum during colonisation of its host sea anemone Exaiptasia diaphana ("Aiptasia"). We also compared the proteome of this native symbiont in the established symbiotic state with that of a non-native symbiont, Durusdinium trenchii. The onset of symbiosis between Aiptasia and Branchioglossum minutum increased accumulation of symbiont proteins associated with acquisition of inorganic carbon and photosynthesis, nitrogen metabolism, micro- and macronutrient starvation, suppression of host immune responses, tolerance to low pH, and management of oxidative stress. Such responses are consistent with a functional, persistent symbiosis. In contrast, D. trenchii predominantly showed elevated levels of immunosuppressive proteins, consistent with the view that this symbiont is an opportunist that forms a less beneficial, less well-integrated symbiosis with this model anemone. By adding symbiont analysis to the already known responses of the host proteome, our results provide a more holistic view of cellular processes that determine host-symbiont specificity and how differences in symbiont partners (i.e., native versus non-native symbionts) may impact the fitness of the cnidarian-dinoflagellate symbiosis.