Impact of Environmental Stressors on the Metabolic Functioning of a Temperate Cnidarian-Dinoflagellate Symbiosis
Cnidarian-dinoflagellate symbioses occur across a wide latitudinal range, from temperate to tropical locations in both hemispheres. In the tropics, this association provides the foundation for the development of highly diverse coral reef ecosystems. Tropical associations are particularly sensitive to thermal variability, however, leading to dysfunction of the relationship and eventual expulsion of the symbiont, known as ‘coral bleaching’. In contrast, temperate associations maintain stable symbiotic relationships in highly fluctuating thermal environments. The reason behind the relative thermal tolerance of temperate associations is still unclear, though the ability to maintain cellular homeostasis through adjustments to metabolic processes is likely a core feature of their resilience. Both a field study and laboratory experiment were conducted to determine the metabolic responses to thermal change of the symbiosis between the temperate anemone Anthopleura aureoradiata and the dinoflagellate Symbiodinium. For the field component, A. aureoradiata were collected from Point Halswell in Wellington Harbour in both summer and winter. For the laboratory experiment, specimens collected at Pautahanui inlet were thermally acclimated in the laboratory, after which temperatures were altered over the course of one week to either 8°C (cold) or 28°C (hot) and maintained at these temperatures for six weeks. Gas chromatography coupled to mass spectrometry was then employed to determine the identity and relative quantity of a wide range of metabolites involved in primary metabolism including organic acids, fatty acids, amino acids and sugars. Based on these data, pathway activity profiling was used to determine the activity of different metabolic pathways both between seasons and in response to cold and heat treatment. A wide range of changes to metabolic processes were observed in both host and symbiont. Photosynthetic capacity was reduced in the symbionts at low temperatures and increased at high temperatures. The only organic acid to be significantly impacted was propanedioic acid, which increased in the host in response to cold treatment, potentially related to increased translocation from the symbiont. Altered fatty acid content in both host and symbiont was related to the role of fatty acids as energy sources and storage compounds and in cell signalling processes. Changes in fatty acid-associated metabolic pathways were exemplified by arachidonic acid and linoleic acid metabolism. Alterations to free amino acids and amino acid related pathways in both host and symbiont were associated with their role as antioxidants and osmoprotectants and the catabolism of amino acids for the production of energy. In symbionts only, altered amino acid content was associated with the role of amino acids in the production of alkaloids. Changes in a number of sugar derivatives in both host and symbiont were associated with their role as antioxidants and osmoprotectants. Altered sugar metabolism in the symbiont clearly indicated an increase in the production of energy rich sugar molecules and production of cellular energy in summer/hot conditions and a decrease in winter/cold conditions. Notably impacted pathways included the Calvin cycle, glycolysis, the pentose phosphate pathway and oxidative phosphorylation. Patterns of sugar related pathway activity in the host were generally opposite to that observed in the symbiont. Overall, prominent but opposing changes in the host and symbiont were detected in the central carbohydrate and energy metabolic pathways. In general, the activity of these pathways increased in the host in winter/cold conditions and decreased in summer/hot conditions, while in the symbiont the pattern was the opposite. These findings highlight the role of metabolic processes in enabling the persistence of a temperate cnidarian-dinoflagellate symbiosis in the face of large temperature fluctuations. This work provides a foundation upon which a deeper understanding of metabolic functioning in the cnidarian-dinoflagellate symbiosis can be built and provides a comparative platform for studies of the more thermally sensitive tropical associations.