Nutritional fluxes in the cnidarian-dinoflagellate symbiosis and the adaptability of corals to climate change

Symbiont diversity could be the answer to ensuring survival of coral reefs in light of a changing climate: changes in symbiont community composition could allow the host to adjust to prevailing environmental conditions. However, this is limited by sub-optimal performance when hosts are paired with non-preferred, i.e. heterologous, symbionts. The potential for cellular integration between host and heterologous symbiont is currently unknown. Here, I explore whether symbiosis function can improve over time when the model cnidarian Aiptasia (Exaiptasia pallida) is inoculated by heterologous symbionts, and the effect of symbiont diversity on host function in juvenile corals (Acropora tenuis). A combined omics approach (proteomics and metabolomics) and stable isotopic labelling were used to establish the potential for improved host-symbiont integration, by elucidating the physiological responses of the hosts, and nutritional exchange between the partners.

In Chapter 2, I characterised the host metabolome and proteome of Aiptasia under thermal stress, when in symbiosis with the homologous Breviolum minutum, or one of the heterologous, but more thermally tolerant symbiont species Durusdinium trenchii and Symbiodinium microadriaticum, over three months in symbiosis. The host metabolome and proteome were symbiont-specific under control conditions, and under thermal stress a clear divide between the host metabolome and proteome of homologous vs. heterologous symbiont-colonised anemones appeared. Differences included reduced carbohydrate stores and increased nitrogen metabolism in hosts paired with heterologous symbiont species compared to B. minutum-colonised hosts, and these were further exacerbated under heat stress. Moreover, heterologous symbionts induced much higher expression of host heat stress proteins (HSPs) and oxidative stress proteins, but suppressed host apoptosis-related proteins. These differences indicate the stressed state of the host when colonised by heterologous symbionts.

In Chapter 3, I investigated the effects of time and repeated thermal stress on the Aiptasia metabolome and proteome with these same symbionts, to assess whether time in symbiosis led to improved symbiosis function. Anemones were left in symbiosis for a total of seven months, while half of the population was exposed to repeated thermal stress and recovery. After this time, no convergence of the host metabolome or proteome was observed between anemones colonised by the heterologous and homologous symbionts. Patterns of protein and metabolite abundance were similar to those described in Chapter 2, with two interesting exceptions. First, anemones containing D. trenchii or S. microadriaticum expressed Niemann-Pick type C (NPC) proteins after three and seven months in symbiosis, respectively; these proteins have previously only been reported in the presence of homologous symbionts. Secondly, S. microadriaticum-colonised hosts contained more glycerol than those containing B. minutum at seven months, perhaps indicating improved metabolic benefit, or alternatively, cellular stress. Symbiosis with these heterologous symbionts therefore showed tentative signs of improvement over time, but only in the absence of thermal stress.

In Chapter 4, I assessed the flux of autotrophic carbon from symbiont to host, and heterotrophic nitrogen from host to symbiont, to determine if time in symbiosis or repeated heat stress events could alter these patterns. Two complementary mass spectrometry methods were used: NanoSIMS, to measure nutrient fluxes at the cellular scale, and IRMS, to measure bulk nutrient fluxes at the holobiont scale. B. minutum-colonised anemones displayed no changes in carbon or nitrogen enrichment with time or thermal regime, even though the cell densities of B. minutum decreased over time (between four and ten months after initial colonisation). By comparison, D. trenchii and S. microadriaticum translocated similar amounts of autotrophic carbon to the host at the cellular scale, but on the holobiont scale did not provide the hosts with as much carbon as B. minutum due to the much higher population density of the homologous symbiont. Additionally, D. trenchii translocated less photosynthate to the host than S. microadriaticum on a cell-specific basis, with this characteristic becoming more pronounced under thermal stress despite photosynthetic function and nitrogen consumption of D. trenchii being unaffected. Thus, D. trenchii seemed to display more opportunistic traits, with these becoming even more pronounced under thermal stress. By comparison, S. microadriaticum could be a more favourable symbiotic partner for Aiptasia, though no evidence was found of improved cellular integration over time, while its consistently low population density limited its overall benefit to the host.

In Chapter 5, I used the coral Acropora tenuis to investigate the effects of symbiont identity and thermal stress on the host proteome, thereby expanding on the model systems approach used elsewhere. Juvenile A. tenuis were inoculated with one of two homologous symbionts: D. trenchii and Cladocopium C1. Four weeks after colonisation, both symbiont species induced increases in host proteins associated with apoptosis, heat stress, and increased metabolic activity under control conditions. Despite these similarities, however, Cladocopium C1 induced a larger change in the host proteome than D. trenchii, with heat stress proteins (HSPs) and proteins involved in apoptosis being more abundant, and cell proliferation-related proteins being less abundant in Cladocopium C1-colonised corals. Under heat stress, the response of A. tenuis was again symbiont-specific. In particular, while D. trenchii is often considered as a thermally tolerant symbiont, corals containing D. trenchii exhibited the largest proteomic response to increased temperature. Indeed, my results suggest that Cladocopium C1 better prepares its host for thermal stress.

Overall, my results provide new insights into the symbiont-specific responses to symbiosis establishment and thermal stress. Additionally, I show the limited possibilities of improved host-symbiont integration over time or in response to repeated thermal stress events, when hosts are paired with heterologous symbiont species. Ultimately, host-symbiont specificity is a severely limiting factor when considering the adaptive potential of corals in response to climate change, highlighting the urgent need for the development of tools for managing the Coral Reef Crisis.