A Compartmental Comparison of Major Lipid Species in a Coral-Symbiodinium Endosymbiosis: Evidence that the Coral Host Regulates Lipogenesis of Its Cytosolic Lipid Bodies

Abstract

The lipid body (LB) formation in the host coral gastrodermal cell cytoplasm is a hallmark of the coral-Symbiodinium endosymbiosis, and such lipid-based entities are not found in endosymbiont-free cnidarian cells. Therefore, the elucidation of lipogenesis regulation in LBs and how it is related to the lipid metabolism of the host and endosymbiont could provide direct insight to understand the symbiosis mechanism. Herein, the lipid composition of host cells of the stony coral Euphyllia glabrescens, as well as that of their cytoplasmic LBs and in hospite Symbiodinium populations, was examined by high performance liquid chromatography (HPLC) and gas chromatography/mass spectrometry (GC/MS), and six major lipid species were identified: wax esters, sterol esters, triacylglycerols, cholesterols, free fatty acids, and phospholipids. Their concentrations differed significantly between host coral cells, LBs, and Symbiodinium, suggesting compartmental regulation. WE were only present in the host coral and were particularly highly concentrated in LBs. Amongst the four species of WE, the monoene R = C18:1/R = C16 was found to be LB-specific and was not present in the host gastrodermal cell cytoplasm. Furthermore, the acyl pool profiles of the individual LB lipid species were more similar, but not equal to, those of the host gastrodermal cells in which they were located, indicating partially autonomous lipid metabolism in these LBs. Nevertheless, given the overall similarity in the host gastrodermal cell and LB lipid profiles, these data suggest that a significant portion of the LB lipids may be of host coral origin. Finally, lipid profiles of the in hospite Symbiodinium populations were significantly distinct from those of the cultured Symbiodinium, potentially suggesting a host regulation effect that may be fundamental to lipid metabolism in endosymbiotic associations involving clade C Symbiodinium.

Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

“…correspond with earlier findings showing that cellular lipid profiles are different in symbiotic versus cultured Symbiodiniaceae in the genus Cladocopium (Chen et al, 2015;Hambleton et al, 2019). Moreover, lipid droplets in the gastrodermal cells of the host were found to be dependent on the symbiotic state of the host (Luo et al, 2009).…”

“…In hospite , Symbiodiniaceae grow 1–2 orders of magnitude slower than in culture (Stambler, ; Wilkerson, Kobayashi, & Muscatine, ), and photosynthesis rates are also depressed (Bhagooli & Hidaka, ; Chen, Yeh, Wang, Li, & Chen, ; Deane & O'Brien, ). Finally, in hospite Symbiodiniaceae have different lipid profiles to those of cultured Symbiodiniaceae (Chen et al, ). Clearly, major morphological, physiological, and biogenesis changes accompany the switch from free‐living to symbiont lifestyle when Symbiodiniaceae algae enter into symbiosis with a host.…”

Uncovering Spatio-Temporal and Treatment-Derived Differences in the Molecular Physiology of a Model Coral-Dinoflagellate Mutualism with Multivariate Statistical Approaches

“…In recent years, a concerted effort has been made to better understand the basic biology of reef-building corals [1][2][3][4], as well as their response to changing environments [5][6][7]; the latter topic is especially pertinent given the extent of the anthropogenic pressures currently facing the high biodiversity ecosystems constructed by these cnidarian-dinoflagellate (genus Symbiodinium) endosymbioses [8,9]. The impact of changing environments on corals is undoubtedly complex, and many species have been shown to acclimate to abiotic regimes previously hypothesized to compromise the integrity of these calcium carbonate-accreting mutualisms.…”

Uncovering Spatio-Temporal and Treatment-Derived Differences in the Molecular Physiology of a Model Coral-Dinoflagellate Mutualism with Multivariate Statistical Approaches

“…In recent years, a concerted effort has been made to better understand the basic biology of reefbuilding corals [1][2][3][4], as well as their response to changing environments [5][6][7]; the latter topic is especially pertinent given the extent of the anthropogenic pressures currently facing the high biodiversity ecosystems constructed by these cnidarian-dinoflagellate (genus Symbiodinium) endosymbioses [8][9]. The impact of changing environments on corals is undoubtedly complex, and many species have been shown to acclimate to extreme abiotic regimes previously hypothesized to compromise the integrity of these calcium carbonate-accreting mutualisms.…”