Hyperthermic stress-induced increase in the expression of glutamate-cysteine ligase and glutathione levels in the symbiotic sea anemone Aiptasia pallida

Abstract

Hyperthermic stress is known to trigger the loss of unicellular algae from a number of symbiotic cnidarians, a phenomenon commonly referred to as bleaching. Oxidative and nitrosative stress have been suggested to play a major role during the process of bleaching, however the underlying molecular mechanisms are still poorly understood. In animals, the intracellular tripeptide glutathione (GSH) is involved in antioxidant defense, redox homeostasis and intracellular redox signaling. Therefore, we tested the hypothesis that hyperthermal stress-induced bleaching in Aiptasia pallida, a model for symbiotic cnidarians, results in increased levels of GSH synthesis. We report the cDNA sequence and functional analysis of the catalytic subunit of glutamate-cysteine ligase (GCLC), which catalyzes the rate-limiting step in GSH biosynthesis. In a time-series experiment, both GCLC gene expression and total GSH levels increased 4-and 1.5-fold, respectively, in response to hyperthermal stress. These results suggest that hyperthermal stress triggers adaptive increases in intracellular GSH biosynthesis in cnidarians as a protective response to oxidative/ nitrosative stress. Our results show the conserved function of GCLC and GSH across animals while placing a new perspective on the role of GSH in redox signaling during cnidarian bleaching.

Metabolite profiling of symbiont and host during thermal stress and bleaching in a model cnidarian-dinoflagellate symbiosis

“…In addition, pools of the antioxidant compound glutathione were elevated in both partners. Glutathione is a tripeptide antioxidant that serves as an important electron donor during oxidative stress in Symbiodinium (Lesser, 2006;Krueger et al, 2014) and in the cnidarian host (Downs et al, 2002;Desalvo et al, 2008;Sunagawa et al, 2008), consistent with the findings of the present study.…”

Differential gene expression in juvenile polyps of the coral Acropora tenuis exposed to thermal and chemical stresses

“…S-adenosylmethionine plays a critical role in the synthesis of glutathione (GSH), one of the most important antioxidants, through its transsulfation pathway (Droge, 2002). Sunagawa et al (2008) suggested that GSH levels in the sea anemone increased 1.5-fold in response to thermal stress. Methionine metabolism in corals may likewise be affected by heat stress.…”

A Profile of an Endosymbiont-enriched Fraction of the Coral Stylophora pistillata Reveals Proteins Relevant to Microbial-Host Interactions

“…Apoptotic elements are similarly induced by hyperthermal stress in the host tissues of the symbiotic sea anemones Anemonia virdis (32), Aiptasia pallida (33,34), and Anthopelura elegantissima (35). Elements of the NF-B signaling pathway of apoptosis in cnidarians are highly conserved traits (36), including genes of the caspase cascade and the pro-apoptotic and antiapoptotic B-cell lymphoma 2 (Bcl-2) family of proteins (33,29) that likely predate the evolution of animal multicellularity via endosymbiotic incorporation of aerobic bacteria as the ancestral proto-mitochondria of unicellular eukaryotes (37).…”