Crude phosphorylation mixtures containing racemic lipid amphiphiles self-assemble to give stable primitive compartments

Dimitri Fayolle, Emiliano Altamura, Alice D'Onofrio, Warren Madanamothoo, Bernard Fenet, Fabio Mavelli, René Buchet, Pasquale Stano, Michele Fiore, Peter Strazewski
2017 Scientific Reports  
et al.. Crude phosphorylation mixtures containing racemic lipid amphiphiles self-assemble to give stable primitive compartments. It is an open question how the chemical structure of prebiotic vesicle-forming amphiphiles complexified to produce robust primitive compartments that could safely host foreign molecules. Previous work suggests that comparingly labile vesicles composed of plausibly prebiotic fatty acids were eventually chemically transformed with glycerol and a suitable phosphate
more » ... into phospholipids that would form robust vesicles. Here we show that phosphatidic acid (PA) and phosphatidylethanolamine (PE) lipids can be obtained from racemic dioleoyl glycerol under plausibly prebiotic phosphorylation conditions. Upon in situ hydration of the crude phosphorylation mixtures only those that contained rac-DOPA (not rac-DOPE) generated stable giant vesicles that were capable of encapsulating watersoluble probes, as evidenced by confocal microscopy and flow cytometry. Chemical reaction sideproducts (identified by IR and MS and quantified by 1 H NMR) acted as co-surfactants and facilitated vesicle formation. To mimic the compositional variation of such primitive lipid mixtures, self-assembly of a combinatorial set of the above amphiphiles was tested, revealing that too high dioleoyl glycerol contents inhibited vesicle formation. We conclude that a decisive driving force for the gradual transition from unstable fatty acid vesicles to robust diacylglyceryl phosphate vesicles was to avoid the accumulation of unphosphorylated diacylglycerols in primitive vesicle membranes. The spontaneous supramolecular self-assembly of amphiphiles to give vesicles is a powerful thermodynamic drive for the emergence of primitive cell-like compartments on the early Earth 1-7 . Fatty acid vesicles are plausible models of primitive cells 8,9 but contemporary cell membranes are based on mixtures of phospholipids, glycolipids and proteins. This elicits the questions about the stepwise transition from very early achiral or racemic amphiphiles to enantiopure glycerophospholipids. It has been argued that the complexification and the compositional evolution of primitive membranes was subjected not only to chemical rules (which chemical transformation is possible?) but also to a sort of supramolecular selection based on the 'performance' of the resulting membranes and whole vesicles -e.g., low critical aggregation (micelle, vesicle) concentration, membrane permeability, capture and retention of non-lipidic organic molecules, membrane growth and vesicle division upon the addition of membrane components, vesicle stability at high magnesium and calcium ions concentrations 8, 9 . Although chemistry suggests several plausible pathways for the stepwise transformation of simple amphiphiles into complex lipids 10-15 , the experimental verifications of the existence, stability, and properties of vesicles composed of plausibly primitive amphiphile mixtures are still limited 9,16-21 . Here we report on primitive membrane systems that originate from crude lipid phosphorylation mixtures. Our starting point is a non-phosphorylated diacylglycerol racemate. Glycerol is a reduced formose C 3 reaction Published: xx xx xxxx OPEN www.nature.com/scientificreports/ 2 SciEnTific REPORTS | (2017) 7:18106 |
doi:10.1038/s41598-017-18053-y pmid:29273739 pmcid:PMC5741756 fatcat:comozlcmwzamtpsgeth63nmrpy