Sphingolipid Metabolism of a Sea Anemone Is Altered by the Presence of Dinoflagellate Symbionts

Abstract

In host-microbe interactions, signaling lipids function in interpartner communication during both the establishment and maintenance of associations. Previous evidence suggests that sphingolipids play a role in the mutualistic cnidarian-Symbiodinium symbiosis. Exogenously applied sphingolipids have been shown to alter this partnership, though endogenous host regulation of sphingolipids by the sphingosine rheostat under different symbiotic conditions has not been characterized. The rheostat regulates levels of pro-survival sphingosine-1-phosphate (S1P) and pro-apoptotic sphingosine (Sph) through catalytic activities of sphingosine kinase (SPHK) and S1P phosphatase (SGPP). The role of the rheostat in recognition and establishment of cnidarian-Symbiodinium symbiosis was investigated in the sea anemone Aiptasia pallida by measuring gene expression, protein levels, and sphingolipid metabolites in symbiotic, aposymbiotic, and newly recolonized anemones. Comparison of two host populations showed that symbiotic animals from one population had lower SGPP gene expression and Sph lipid concentrations compared to aposymbiotic animals, while the other population had higher S1P concentrations than their aposymbiotic counterparts. In both populations, the host rheostat trended toward host cell survival in the presence of symbionts. Furthermore, upregulation of both rheostat enzymes on the first day of host recolonization by symbionts suggests a role for the rheostat in host-symbiont recognition during symbiosis onset. Collectively, these data suggest a regulatory role of sphingolipid signaling in cnidarian-Symbiodinium symbiosis and symbiont uptake.

Spatial metabolomics for symbiotic marine invertebrates

“…Sphingolipids can accumulate in host microalgal symbiont-containing gastrodermal cells of the sea anemone Exaiptasia diaphana. However, contrary to expectations, LC-MS/MS analysis of homogenized tissues did not reveal a significant sphingolipid concentration difference between anemones exposed to different light/dark treatments, possibly due to the dilution effect of non-symbiotic cells (Kitchen et al, 2017). These examples highlight that spatial knowledge of molecular species is key for obtaining in-depth understanding of host-microbe interactions.…”

“…Ceramides are intermediates in the biosynthesis and metabolism of all sphingolipids — a class of lipids that are important constituents of biological membranes which function in cell signaling through the activation of specific G-protein-coupled receptors — regulating processes such as apoptosis, cell survival, inflammation, autophagy and oxidative stress responses (Bhattacharya, 2022; Rosset et al , 2021). The sphingosine rheostat refers to the balance in cellular concentrations of pro-survival sphingolipids (i.e., sphingosine-1-phosphate; S1P) and pro-apoptotic sphingolipids (i.e., sphingosine and ceramide), which is a homeostatic process that determines cell fate (Kitchen et al , 2017; Rosset et al, 2021) (Fig. 3).…”

Tentacle patterning during Exaiptasia diaphana pedal lacerate development differs between symbiotic and aposymbiotic animals

“…A major advantage of using Aiptasia as a lab model is the ability to maintain adults in the lab without any symbiotic dinoflagellates ( Weis et al, 2008 ; Voolstra, 2013 ; Matthews et al, 2016 ). These aposymbiotic (Apo) anemones can be used as a comparison to symbiotic (Sym) anemones to assess the influence of nutritional and symbiotic status on molecular, cellular, physiological and metabolic processes ( Lehnert et al, 2014 ; Carlisle, Murphy & Roark, 2017 ; Kitchen, Poole & Weis, 2017 ; Matthews et al, 2017 ; Rädecker et al, 2018 ; Sorek et al, 2018 ). Furthermore, Apo anemones can be re-inoculated with Symbiodiniaceae to understand how colonization is influenced by different symbiont species or under different environmental conditions ( Neubauer et al, 2017 ; Gabay, Weis & Davy, 2018 ; Parkinson et al, 2018 ; Matthews et al, 2018 ; Sproles et al, 2020 ; Herrera et al, 2021 ).…”

Symbiosis with Dinoflagellates Alters Cnidarian Cell-Cycle Gene Expression

“…In A. elegantissima, the presence of symbionts resulted in a decrease in the expression of four host genes involved in host cell apoptosis and an increase in the expression of one host gene involved in host cell proliferation through an impact on the sphingosine-1-phosphate (S1P) and prohibitin pathways [37]. In Aiptasia, S1P has been shown to promote host cell survival both during association with symbionts [42] and periods of host stress [43]. However, we still have a long way to go to understand which host genes are altered in their expression in the presence of symbionts and how this induces downstream effects on host growth.…”