Nitrogen-deprivation elevates lipid levels in Symbiodinium spp. by lipid droplet accumulation: morphological and compositional analyses.
Stable cnidarian-dinoflagellate (genus Symbiodinium) endosymbioses depend on the regulation of nutrient transport between Symbiodinium populations and their hosts. It has been previously shown that the host cytosol is a nitrogen-deficient environment for the intracellular Symbiodinium and may act to limit growth rates of symbionts during the symbiotic association. This study aimed to investigate the cell proliferation, as well as ultrastructural and lipid compositional changes, in free-living Symbiodinium spp. (clade B) upon nitrogen (N)-deprivation. The cell proliferation of the N-deprived cells decreased significantly. Furthermore, staining with a fluorescent probe, boron dipyrromethane 493/503 (BODIPY 493/503), indicated that lipid contents progressively accumulated in the N-deprived cells. Lipid analyses further showed that both triacylglycerol (TAG) and cholesterol ester (CE) were drastically enriched, with polyunsaturated fatty acids (PUFA; i.e., docosahexaenoic acid, heneicosapentaenoic acid, and oleic acid) became more abundant. Ultrastructural examinations showed that the increase in concentration of these lipid species was due to the accumulation of lipid droplets (LDs), a cellular feature that have previously shown to be pivotal in the maintenance of intact endosymbioses. Integrity of these stable LDs was maintained via electronegative repulsion and steric hindrance possibly provided by their surface proteins. Proteomic analyses of these LDs identified proteins putatively involved in lipid metabolism, signaling, stress response and energy metabolism. These results suggest that LDs production may be an adaptive response that enables Symbiodinium to maintain sufficient cellular energy stores for survival under the N-deprived conditions in the host cytoplasm.
Graduate Institute of Marine Biotechnology, National Dong-Hwa University, Pingtung, Taiwan ; Taiwan Coral Research Center, National Museum of Marine Biology and Aquarium, Pingtung, Taiwan.
Pei-Luen
PL
Jiang
Graduate Institute of Biotechnology, National Chung-Hsing University, Taichung, Taiwan.
Buntora
B
Pasaribu
Graduate Institute of Marine Biotechnology, National Dong-Hwa University, Pingtung, Taiwan ; Taiwan Coral Research Center, National Museum of Marine Biology and Aquarium, Pingtung, Taiwan ; Department of Marine Biotechnology and Resources, National Sun Yat-Sen University, Kaohsiung, Taiwan.
Chii-Shiarng
CS
Chen
D000220:Adaptation, Biological / Q000502:physiology*; D000818:Animals; D015153:Blotting, Western; D001896:Boron Compounds; D049109:Cell Proliferation; D002734:Chlorophyll / Q000378:metabolism; D000077194:Chlorophyll A; D002788:Cholesterol Esters / Q000378:metabolism; D003063:Cnidaria / Q000382:microbiology*; D003600:Cytosol / Q000378:metabolism*; D004141:Dinoflagellida / Q000235:genetics / Q000254:growth & development* / Q000648:ultrastructure; D004591:Electrophoresis, Polyacrylamide Gel; D008401:Gas Chromatography-Mass Spectrometry; D054884:Host-Pathogen Interactions; D050356:Lipid Metabolism / Q000502:physiology*; D046529:Microscopy, Electron, Transmission; D008856:Microscopy, Fluorescence; D009584:Nitrogen / Q000172:deficiency; D009841:Oligonucleotides / Q000235:genetics; D012394:Rosaniline Dyes; D013045:Species Specificity; D013559:Symbiosis; D014280:Triglycerides / Q000378:metabolism
C527198:4,4-difluoro-1,3,5,7,8-pentamethyl-4-bora-3a,4a-diaza-s-indacene; D001896:Boron Compounds; D002788:Cholesterol Esters; D009841:Oligonucleotides; D012394:Rosaniline Dyes; D014280:Triglycerides; D002734:Chlorophyll; C048139:Coomassie blue; D009584:Nitrogen; D000077194:Chlorophyll A