Mapping carbon fate during bleaching in a model cnidarian symbiosis: the application of ¹³C metabolomics

Abstract

Coral bleaching is a major threat to the persistence of coral reefs. Yet we lack detailed knowledge of the metabolic interactions that determine symbiosis function and bleaching-induced change. We mapped autotrophic carbon fate within the free metabolite pools of both partners of a model cnidarian-dinoflagellate symbiosis (Aiptasia-Symbiodinium) during exposure to thermal stress via the stable isotope tracer ( C bicarbonate), coupled to GC-MS. Symbiont photodamage and pronounced bleaching coincided with substantial increases in the turnover of non C-labelled pools in the dinoflagellate (lipid and starch store catabolism). However, C enrichment of multiple compounds associated with ongoing carbon fixation and de novo biosynthesis pathways was maintained (glucose, fatty acid and lipogenesis intermediates). Minimal change was also observed in host pools of C-enriched glucose (a major symbiont-derived mobile product). However, host pathways downstream showed altered carbon fate and/or pool composition, with accumulation of compatible solutes and nonenzymic antioxidant precursors. In hospite symbionts continue to provide mobile products to the host, but at a significant cost to themselves, necessitating the mobilization of energy stores. These data highlight the need to further elucidate the role of metabolic interactions between symbiotic partners, during the process of thermal acclimation and coral bleaching.

Resolving coral photoacclimation dynamics through coupled photophysiological and metabolomic profiling

“…Such direct measurements of coral metabolism could help improve understanding of the potential effects of high light on carbon fixation and translocation. Furthermore, there is also evidence to suggest that studies of in vitro Symbiodiniaceae may overestimate the importance of glycerol, and glucose is in fact the major photosynthate translocated from in hospite symbionts to hosts (Ishikura et al, 1999;Hillyer et al, 2017b;Matthews et al, 2017). Glucose concentration was not found to vary between LL to HL and LL to LL control corals in the present study.…”

Experimentally Induced Bleaching in the Sea Anemone Exaiptasia Supports Glucose as a Main Metabolite Associated with Its Symbiosis

“…The consistency of our results with the literature [13,36,45] strongly supports the hypothesis that glucose is a major chemical form in the translocation of reduced carbon in the symbiosis of E. pallida. The possibility of glucose being synthesized from glycerol seems unlikely, being an energyconsuming path.…”

“…In contrast, thermally induced bleaching seems to have a minor effect on glucose metabolism for this anemone, as has been shown by Hillyer et al [36].…”

Transcriptomic insights into the establishment of coral-algal symbioses from the symbiont perspective

“…Glucose is thought to be the major photosynthetic product translocated from the algal symbiont to its cnidarian host (Burriesci et al, 2012; Hillyer et al, 2017). Results presented here suggest that, whereas in free-living Symbiodiniaceae fixed carbon in excess of immediate requirements likely accumulates in glycogen and/or starch, in symbiosis the balance shifts to glycogen / starch breakdown; limit dextrinase is upregulated to enable glucose mobilization, glycogen synthase is downregulated and the carbohydrate transporter R144.6 is activated.…”