The sphingosine rheostat is involved in the cnidarian heat stress response but not necessarily in bleaching

Abstract

Sphingolipids play important roles in mitigating cellular heat and oxidative stress by altering membrane fluidity, receptor clustering and gene expression. Accumulation of signaling sphingolipids that comprise the sphingosine rheostat, pro-apoptotic sphingosine (Sph) and pro-survival sphingosine-1-phosphate (S1P) is key to determining cell fate. Reef-building corals and other symbiotic cnidarians living in shallow tropical waters can experience elevated seawater temperature and high UV irradiance, two stressors that are increasing in frequency and severity with climate change. In symbiotic cnidarians, these stressors disrupt the photosynthetic machinery of the endosymbiont and ultimately result in the collapse of the partnership (dysbiosis), known as cnidarian bleaching. In a previous study, exogenously applied sphingolipids altered heat-induced bleaching in the symbiotic anemone Aiptasia pallida, but endogenous regulation of these lipids is unknown. Here, we characterized the role of the rheostat in the cnidarian heat stress response (HSR) and in dysbiosis. Gene expression of rheostat enzymes sphingosine kinase (AP-SPHK) and S1P phosphatase (AP-SGPP), and concentrations of sphingolipids were quantified from anemones incubated at elevated temperatures. We observed a biphasic HSR in A. pallida. At early exposure, rheostat gene expression and lipid levels were suppressed while gene expression of a heat stress biomarker increased and 40% of symbionts were lost. After longer incubations at the highest temperature, AP-SGPP and then Sph levels both increased. These results indicate that the sphingosine rheostat in A. pallida does not participate in initiation of dysbiosis, but instead functions in the chronic response to prolonged heat stress that promotes host survival.

Free‐living and symbiotic lifestyles of a thermotolerant coral endosymbiont display profoundly distinct transcriptomes under both stable and heat stress conditions

“…The sphingosine rheostat describes the interconversion between sphingosine and sphingosine 1‐phosphate (Cuvillier et al, ), which serve as critical signalling lipids in cell death and proliferation, respectively. Sphingolipid regulation has long been implicated in symbiosis from the host perspective (Rodriguez‐Lanetty et al, ); stable symbiosis is associated with the rheostat shifted towards sphingosine 1‐phosphate (Detournay & Weis, ; Kitchen & Weis, ). However, the symbiont side of sphingolipid changes under stress and symbiosis has not previously been described.…”

“…Sphingolipid regulation has long been implicated in symbiosis from the host perspective (Rodriguez-Lanetty et al, 2006); stable symbiosis is associated with the rheostat shifted towards sphingosine 1-phosphate (Detournay & Weis, 2011;Kitchen & Weis, 2017).…”

Elucidating gene expression adaptation of phylogenetically divergent coral holobionts under heat stress

“…Aminoglycan catabolism, keratan sulfate catabolic process, and sphingolipid metabolism were downregulated in all host species (Supplementary Data 3). Sphingolipid metabolism has been also documented as a part of a rheostat involved in the cnidarian heat stress response 24 . Consistent with the DEG orthology analysis, a large number of enriched GO terms is conserved in the closely related species, O. faveolata and P. clivosa when compared to S. radians.…”

The nitrogen-fixing symbiotic cyanobacterium,Nostoc punctiformecan regulate plant programmed cell death

“…1b). In a diverse range of bacteria-eukaryote symbioses, bacterial symbionts are known to produce molecules ('symbiosis signals') which maintain cellular homeostasis and suppress host PCD (An et al, 2014;Kitchen and Weis, 2017;Pannebakker et al, 2007).…”