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Biogenesis, dynamic and homeostasis of membrane lipids

Published on 13 February 2019

In eukaryotic cells, each membrane has a specific lipid composition (or lipid profile). The general question investigated by the team is to decipher the molecular processes responsible for the establishment and maintenance of glycerolipid profiles, in membranes and lipid droplets, in plastid-containing eukaryotes (plants and algae).

Glycerolipids are made by the assembly of fatty acids (FAs), glycerol and polar heads. Less than a dozen classes of glycerolipids are sufficient to compose most biological membranes, including phospholipids such as phosphatidylcholine (PC), phosphatidylethanolamine (PE), the major constituents of extra-plastidial membranes, and non-phosphorous galactolipids, such as monogalactosyldiacylglycerol (MGDG) or digalactosyldiacylglycerol (DGDG), which form the bulk of photosynthetic membranes (Figure 1). In algae, there is a third type of membrane glycerolipids, also non-phosphorous, called betaine lipids and localized in extraplastidial membranes.

Figure 1 : Glycerolipid, constituents of biological membranes and oils. Glycerolipids are a specific group of lipids, consisting of a glycerol backbone to which 1 to 3 fatty acids are linked by an ester bond. Glycerolipids containing two fatty acids may have a polar head, and are used to build bilayers, forming the matrix of biological membranes. Glycerolipids containing three fatty acids are called triacylglycerols, or oils, and accumulate in the form of droplets within the cells.

In plants, the biosynthesis of glycerolipids schematically responds to 4 rules:
- The biosynthesis of fatty acids takes place in the stroma of the chloroplast;
- The assembly of fatty acids and glycerol to form most of the phospholipids takes place in the endoplasmic reticulum (ER);
- The synthesis of galactolipids, sulfolipid and some of the phosphatidylglycerol takes place in the plastid envelope;
- The membrane glycerolipids can finally be converted into triacylglycerol (TAG), a reserve lipid stored in lipid droplets.
Consequently, the lipid composition of a membrane depends on 3 major phenomena: (1) the neosynthesis of glycerolipids; (2) the conversion between glycerolipids, by exchanges of fatty acids or polar heads and finally (3) the glycerolipid transport/trafficking within the cell. The proportions in lipid classes in each membrane are very stable. In physiological terms, these steady states correspond to a complex series of processes called “membrane lipid homeostasis”, which provides the framework for the research lines in the team.

Our work is in line with the past research of the team, i.e. advancing knowledge of the processes setting up the membrane lipid distribution in plastid-containing eukaryotes at steady state (membrane lipid homeostasis) and tuning this steady state in response to environmental changes (lipid remodeling). The overall strategy remains to consider the glycerolipid metabolic scheme as a system, and to contribute to the international effort to characterize its components and dynamics by a multidisciplinary approach. Our questions will focus on eukaryotes containing plastid derived from primary or secondary endosymbiosis. Our team has a solid knowledge of plant lipid metabolism.

- In our model of primary endosymbiont (Arabidopsis), lipid synthesis and conversion enzymes are well known but, as in other eukaryotes, lipid trafficking and sorting systems are still barely understood and represent therefore the next critical gap in knowledge.

- For organisms deriving from secondary endosymbiosis (Phaeodactylum, Nannochloropsis), the background knowledge is very weak and all the bases of the lipid metabolism need to be investigated.

Our challenging scientific issues for the future include
1) the characterization of the lipid trafficking systems and fluxes,
2) the deciphering of the role and the control of glycerolipid homeostasis within the whole system,
3) the reconstruction of membrane lipid pathways and
4) the relationship between lipid biosynthesis and membrane expansion and architecture.
Concerning the translation of knowledge for applied sciences, the control of TAG accumulation should be sought through the development of chemical genetics and synthetic biology approaches, in a rigorous collaborative context with industrial partners. To achieve these goals, the team will rely on the research projects of each P.I. of the team, the access to a unique lipidomics platform, the development of cutting-edge electron microscopy methods, and the existence of two project teams involved in industrial partnership. Three main research axes will drive our research (Figure 2):
Homeostasis of glycerolipids in secondary endosymbionts (Phaeodactylum, Nannochloropsis, Aurantiochytrium),
Lipid trafficking in photosynthetic primary endosymbionts (Arabidopsis),
Remodeling of glycerolipids in microalgae and plants in response to abiotic parameters, including those characterizing alpine environments.

Figure 2. Research model and research axis of the team.