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Particularly tacky sweet lipids on the surface of photosynthetic membranes

Researchers from our Laboratory [collaboration] reveal the essential role of sugars harbored by lipids in the cohesive force between adjacent membranes. This study was published on 3 April 2017 in the journal Nature Communications.

Published on 21 April 2017
Life on our planet depends on photosynthesis, a complex biological process combining the capture of solar energy with the use of this energy to convert carbon dioxide from the air into organic matter. Photosynthetic organisms range from the simplest unicellular forms, such as cyanobacteria, to algae and plants, and thus provide organic matter at the base of the food chain of ecosystems. At the subcellular level, photosynthetic membranes form the solar pannels, and consist of flattened membrane sacs, stacked in such large numbers that the overall surface area of these membranes in one square meter of leaves is on the order of 1 to 3 times the surface area of a rugby stadium. A mystery is to understand the construction of these flattened cisternae, and then understand their stacking.

An important factor for these two phenomena is the interaction between adjacent membranes. These biological membranes are composed of a matrix of polar lipids into which proteins are inserted, in particular the proteins involved in the photosynthesis process (Figure A).

Figure A: Components in a biological membrane.
© Juliette Jouhet

To date, lipids are just considered for their role as a fluid matrix, allowing proteins to move laterally. The most common hypothesis for flattening and stacking membranes is that spherical vesicles form initially, grow into flattened sacs without understanding how this flattening occurs, and then stack thanks to adhesion forces provided only by proteins. There are cases where the photosynthetic membranes are stacked in the absence of these proteins. Intriguingly, four lipids are conserved in all photosynthetic membranes, from cyanobacteria to algae and plants, in particular digalactosyldiacylglycerol (DGDG) (Figure B). 

Figure B: DGDG (digalactosyldiacylglycerol): a lipid conserved in photosynthetic membranes from cyanobacteria to algae and plants.
© Juliette Jouhet

Biophysical work carried out previously in collaboration between two laboratories in Grenoble, ours and the Laue Langevin Institute, using neutron reflectometry, had shown that DGDG made biological membranes cohesive with each other. The cohesive strength due to DGDG was remarkably high, as it compensated for example the electromagnetic repulsion exerted by negatively charged lipids mixed with DGDG. The understanding of the adhesion forces exerted between the sugar residues harbored by DGDG (Figure C) came from molecular modeling and simulations, carried out in collaboration with the Berlin Helmholtz Center for Matter and Energy, The Free University of Berlin, the University of Groningen and the Max Planck Institute on Colloids and Interfaces, Potsdam. 

Figure B: DGDG-driven membrane interactions.
© Juliette Jouhet

This work published in Nature Communications thus shows how a lipid contributes significantly to the architecture of photosynthetic membranes, giving an explanation for its conservation during evolution, and opens perspectives to exploit sugar residues for the elaboration of stacked biomimetic membranes.

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