Differential distribution of lipids in epidermis, gastrodermis and hosted Symbiodinium in the sea anemone Anemonia viridis

Wang

et al. 2017

Sci Rep

Lipid bodies (LBs) in the coral gastrodermal tissues are key organelles in the regulation of endosymbiosis and exhibit a diel rhythmicity. Using the scleractinian Euphyllia glabrescens collected across the diel cycle, we observed temporally dynamic lipid profiles in three cellular compartments: host coral gastrodermal cells, LBs, and in hospite Symbiodinium. Particularly, the lipidome varied over time, demonstrating the temporally variable nature of the coral–Symbiodinium endosymbiosis. The lipidome-scale data highlight the dynamic, light-driven metabolism of such associations and reveal that LBs are not only lipid storage organelles but also act as a relay center in metabolic trafficking. Furthermore, lipogenesis in LBs is significantly regulated by coral hosts and the lipid metabolites within holobionts featured predominantly triacylglycerols, sterol esters, and free fatty acids. Given these findings through a time-varied lipidome status, the present study provided valuable insights likely to be crucial to understand the cellular biology of the coral–Symbiodinium endosymbiosis.

Section: Discussionsupporting

confidence: 90%

“…Possible trafficked lipids and FA moieties from Symbiodinium to the host 10, 44 , or host to Symbiodinium 49 have been studied in hard corals for decades. However, the direct translocation of lipids and lipogenesis among LBs, coral host and Symbiodinium has not been reported 9, 12, 47 .…”

Section: Discussionmentioning

confidence: 98%

Coral lipid bodies as the relay center interconnecting diel-dependent lipidomic changes in different cellular compartments

Wang

et al. 2017

Sci Rep

“…We detected a large decline in pools of the nonlabelled fraction only of both C12:0 and C14:0, with little change in pools of the labelled fraction, suggesting a source other than change in input from de novo synthesis. Further, we observed little change to the enrichment of pools of downstream long‐chain fatty acids C16:0, C18:1, C18:0 and C22:0, which form the more major components of structural lipids, such as those associated with lipid membranes (Kneeland et al ., ; Revel et al ., ).…”

Section: Discussionmentioning

confidence: 97%

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

et al. 2017

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.

“…Several hypotheses can be proposed to explain the maintenance of npc2 duplicated genes in symbiotic cnidarians. Recent studies have suggested that cnidarians must obtain cholesterol directly from dietary intake or from their dinoflagellate symbionts (Revel et al, ; Treignier, Grove, Ferrier‐Pages, & Tolosa, ). NPC proteins may therefore be involved in sterol acquisition from the symbionts by the cnidarian host (Baumgarten et al, ; Lehnert et al, ).…”

Section: Discussionmentioning

confidence: 99%

Expression patterns of sterol transporters NPC1 and NPC2 in the cnidarian-dinoflagellate symbiosis

Dani

Priouzeau

Mertz

et al. 2017

Cellular Microbiology

Self Cite

The symbiotic interaction between cnidarians (e.g., corals and sea anemones) and photosynthetic dinoflagellates of the genus Symbiodinium is triggered by both host-symbiont recognition processes and metabolic exchange between the 2 partners. The molecular communication is crucial for homeostatic regulation of the symbiosis, both under normal conditions and during stresses that further lead to symbiosis collapse. It is therefore important to identify and fully characterise the key players of this intimate interaction at the symbiotic interface. In this study, we determined the cellular and subcellular localization and expression of the sterol-trafficking Niemann-Pick type C proteins (NPC1 and NPC2) in the symbiotic sea anemones Anemonia viridis and Aiptasia sp. We first established that NPC1 is localised within vesicles in host tissues and to the symbiosome membranes in several anthozoan species. We demonstrated that the canonical NPC2-a protein is mainly expressed in the epidermis, whereas the NPC2-d protein is closely associated with symbiosome membranes. Furthermore, we showed that the expression of the NPC2-d protein is correlated with symbiont presence in healthy symbiotic specimens. As npc2-d is a cnidarian-specific duplicated gene, we hypothesised that it probably arose from a subfunctionalisation process that might result in a gain of function and symbiosis adaptation in anthozoans. Niemann-Pick type C proteins may be key players in a functional symbiosis and be useful tools to study host-symbiont interactions in the anthozoan-dinoflagellate association.