Are Niemann‐Pick type C proteins key players in cnidarian–dinoflagellate endosymbioses?

Abstract

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.

Aiptasia sp. larvae as a model to reveal mechanisms of symbiont selection in cnidarians

“…Recent transcriptomic and proteomic approaches in different systems have identified a set of symbiosis-specific candidate genes, and we found many similar genes among our list of differentially expressed genes (DEG); for example, the lysosomal Niemann-Pick disease type C2 (NPC2) protein2838; transmembrane receptors that may play a role in symbiont recognition293940; and small GTPases potentially involved in endocytotic vesicle transport during phagocytosis414243 (Fig. 5).…”

Transcriptomic differences between day and night in Acropora millepora provide new insights into metabolite exchange and light‐enhanced calcification in corals

“…; Dani et al . ). These data are consistent with the observation that fatty acid and sterol content in coral tissue are affected by both light and food availability (Treignier et al .…”

Transcriptome analysis illuminates the nature of the intracellular interaction in a vertebrate-algal symbiosis

“…One differentially expressed algal gene that may be implicated in nutrient exchange with salamander cells is an algal gene with homology to Niemann-Pick type C (NPC) proteins, which is more highly expressed in intracellular algae. These proteins are involved in intracellular cholesterol transport, and are potential mediators of lipid transfer in cnidarian-dinoflagellate endosymbioses (Dani et al, 2014). Intriguingly, increased expression of this potential sterol sensing gene is observed in our intracellular algal transcripts, whereas in cnidarian-dinoflagellate interactions it is the host that utilizes NPC proteins (Dani et al, 2014).…”