Fatty Acid and Phospholipid Syntheses Are Prerequisites for the Cell Cycle of Symbiodinium and Their Endosymbiosis within Sea Anemones

Li-Hsueh Wang,Hsieh-He Lee,Lee-Shing Fang,Anderson B Mayfield,Chii-Shiarng Chen,Eric Cascales

doi:10.1371/journal.pone.0072486

Abstract

Lipids are a source of metabolic energy, as well as essential components of cellular membranes. Although they have been shown to be key players in the regulation of cell proliferation in various eukaryotes, including microalgae, their role in the cell cycle of cnidarian-dinoflagellate (genus Symbiodinium) endosymbioses remains to be elucidated. The present study examined the effects of a lipid synthesis inhibitor, cerulenin, on the cell cycle of both cultured Symbiodinium (clade B) and those engaged in an endosymbiotic association with the sea anemone Aiptasia pulchella. In the former, cerulenin exposure was found to inhibit free fatty acid (FFA) synthesis, as it does in other organisms. Additionally, while it also significantly inhibited the synthesis of phosphatidylethanolamine (PE), it did not affect the production of sterol ester (SE) or phosphatidylcholine (PC). Interestingly, cerulenin also significantly retarded cell division by arresting the cell cycles at the G0/G1 phase. Cerulenin-treated Symbiodinium were found to be taken up by anemone hosts at a significantly depressed quantity in comparison with control Symbiodinium. Furthermore, the uptake of cerulenin-treated Symbiodinium in host tentacles occurred much more slowly than in untreated controls. These results indicate that FFA and PE may play critical roles in the recognition, proliferation, and ultimately the success of endosymbiosis with anemones.

Highlights

Lipids are important components of all living organisms, as they are a source of metabolic energy and serve as essential components of cellular membranes
Our current study focused on the ability of cerulenin-treated Symbiodinium to infect sea anemones, aiming to elucidate the role of lipid synthesis in the establishment of anemone-dinoflagellate endosymbiosis
To determine the optimal concentration of cerulenin required to interfere with the cell cycle progression, cerulenin was added at T00 in three different concentrations: 1027, 1026, or 1025 M (Fig. 3a)

Summary

Introduction

Lipids are important components of all living organisms, as they are a source of metabolic energy and serve as essential components of cellular membranes. They are involved in processes such as cell proliferation, cell differentiation, and organ morphogenesis, which are all intimately associated with the progression of the cell cycle [1]. Polar glycerolipids (glycolipid, phosolipid, and ether lipid) are synthesized sequentially during the cell cycle of Chlamydomonas reinhardtii [3]. Crypthecodinium cohnii, cells exhibit a stepwise increase in polar lipids and a continuous increase in neutral lipids over the course of the cell cycle [4]. The same study showed that inhibiting lipid synthesis caused cell cycle arrest at the early G1 phase, not the G2/ M phase, demonstrating the essential role of lipid synthesis in regulating cell cycle progression

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Results

Conclusion