Abstract
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.
Highlights
Symbiodinium spp., a unicellular dinoflagellate, is commonly found in mutualistic associations with invertebrates such as corals and anemones, and able to transfer more than 90% of its photosynthetically fixed carbon to the host cytoplasm in which it resides [1]
Cells cultivated in the nitrogendeprived medium proliferated more slowly than those cultivated in the normal medium, after three days of experimentation (Fig. 1A)
In Symbiodinium grown in control medium, little lipid accumulation was observed as shown by very dim BODIPY staining (Fig. 1B)
Summary
Symbiodinium spp., a unicellular dinoflagellate, is commonly found in mutualistic associations with invertebrates such as corals and anemones, and able to transfer more than 90% of its photosynthetically fixed carbon to the host cytoplasm in which it resides [1]. This intracellular symbiosis (i.e. the endosymbiosis) has been the focus of intensive research due to its pivotal role in maintaining the health of corals and homeostasis of the marine ecosystem. The supply of organic carbon by Symbiodinium to the hosts and the recycling of essential nutrients during such associations have contributed to the success of coral reefs in nutrient-limited tropical seas [3]. Nitrogen, which is one of the most important essential nutrients, can be excreted as ammonium by the host [6]
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