Thermal and menthol stress induce different cellular events during sea anemone bleaching

Abstract

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

Symbiont Chloroplasts Remain Active During Bleaching-Like Response Induced by Thermal Stress in Collozoum pelagicum (Collodaria, Retaria)

“…In the autophagic pathway, the target is enveloped in a membrane structure before lysosomal fusion, which initiates digestion by hydrolytic enzymes (Cuervo, 2004). Both apoptosis and autophagy have been observed during cnidarian bleaching and can occur simultaneously (Dunn et al, 2007) or alternatively in response to hyperthermal stress (Richier et al, 2006;Dani et al, 2016). In addition, another process related to symbiotic dinoflagellate autophagy has been reported in cnidarians and is referred to as "symbiophagy, " which results in the digestion of the resident dinoflagellates (Downs et al, 2009).…”

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

“…In this study, we characterised both the abundance and localisation, at the cellular and subcellular levels, of NPC1, NPC2‐a, and NPC2‐d proteins in the cnidarian–dinoflagellate symbiosis. We applied both “normal” conditions and hyperthermal stress, to test the impacts of symbiosis dysfunction/“bleaching”; we also compared the impacts of menthol treatment, which causes host autophagy (Dani et al, ) and produces “healthy” aposymbiotic hosts (Matthews et al, ; Wang, Chen, Tew, Meng, & Chen, ). We demonstrated that NPC1 is localised both within vesicles in host tissues and to the perisymbiont membrane.…”

Differential gene expression analysis of symbiotic and aposymbiotic Exaiptasia anemones under immune challenge with Vibrio coralliilyticus

“…These include menthol (Wang, Chen, Tew, Meng, & Chen, 2012) and photosynthesis inhibitors (Jones, 2004) that result in bleaching. Several mechanisms have been identified that result in the degradation and expulsion of the symbionts, including apoptosis, necrosis, and symbiont digestion via autophagy (symbiophagy; Dani et al, 2016), and the mechanisms vary depending on the type of stress. Apoptosis and necrosis predominate in heat-stress bleaching, while symbiophagy predominates in menthol bleaching (Dani et al, 2016;Wang et al, 2012).…”

“…Apoptosis and necrosis predominate in heat-stress bleaching, while symbiophagy predominates in menthol bleaching (Dani et al, 2016;Wang et al, 2012). Arrest of phagosomal maturation is required for the establishment of symbiosis, and Dani et al (2016) suggest that a re-engagement of phagosomal maturation is involved in the breakdown.…”