The symbiotic interaction between cnidarians, such as corals and sea anemones, and the unicellular algae Symbiodinium is regulated by yet poorly understood cellular mechanisms, despite the ecological importance of coral reefs. These mechanisms, including host-symbiont recognition and metabolic exchange, control symbiosis stability under normal conditions, but also lead to symbiosis breakdown (bleaching) during stress. This study describes the repertoire of the sterol-trafficking proteins Niemann-Pick type C (NPC1 and NPC2) in the symbiotic sea anemone Anemonia viridis. We found one NPC1 gene in contrast to the two genes (NPC1 and NPC1L1) present in vertebrate genomes. While only one NPC2 gene is present in many metazoans, this gene has been duplicated in cnidarians, and we detected four NPC2 genes in A. viridis. However, only one gene (AvNPC2-d) was upregulated in symbiotic relative to aposymbiotic sea anemones and displayed higher expression in the gastrodermis (symbiont-containing tissue) than in the epidermis. We performed immunolabelling experiments on tentacle cross sections and demonstrated that the AvNPC2-d protein was closely associated with symbiosomes. In addition, AvNPC1 and AvNPC2-d gene expression was strongly downregulated during stress. These data suggest that AvNPC2-d is involved in both the stability and dysfunction of cnidarian-dinoflagellate symbioses.
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.
International audienceCnidarian-dinoflagellate symbiosis disruption and subsequent bleaching are major concerns, especially regarding their ecological consequences on coral reefs and temperate coralligenous communities. Cnidarian bleaching is caused by a variety of environmental stressors, such as elevated seawater temperature associated with global climate change, and by pollutants, such as herbicides and metals. Several cellular events have been described to explain symbiosis dysfunction and bleaching. Excess or damaged Symbiodinium symbionts are removed through a variety of mechanisms, including exocytosis, apoptosis, necrosis and autophagy. However, few studies have compared in the same species the relative involvement of these mechanisms, according to the stress inducing the bleaching. In this study, we used two different treatments —temperature and menthol— to induce bleaching in the sea anemone Anemonia viridis. By monitoring the ultrastructural tissue modifications, in control specimens we observed a basal rate of in situ symbiont digestion —or symbiophagy— induced by starvation. Symbiophagy was strongly induced in menthol-treated specimens and was the main cellular process of bleaching, whereas apoptosis and necrosis predominated in hyperthermal-induced bleaching. These results suggested a host effect through autophagy in menthol-treated specimens. These observations also suggested that symbiont removal may result from reengagement of the phagosomal maturation process in the host. These overall data demonstrate that several Symbiodinium cell removal mechanisms coexist and that stressors can activate one or more of these pathways, depending on the stress type, intensity or duration
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