Fatty acid membrane assembly on coacervate microdroplets as a step towards a hybrid protocell model

• Published in: Nature chemistry 2014-06, Vol.6 (6), p.527-533
• Main Authors: Dora Tang, T-Y., Rohaida Che Hak, C., Thompson, Alexander J., Kuimova, Marina K., Williams, D. S., Perriman, Adam W., Mann, Stephen
• Format: Article
• Language: English
• Subjects: 639/638/204/904; Adenosine triphosphate; Adenosine Triphosphate - chemistry; Analytical Chemistry; Artificial Cells; ATP; Biochemistry; Catalysis; Cell Membrane - chemistry; Chemistry; Chemistry/Food Science; Emulsions; Fatty acids; Fatty Acids - chemistry; Inorganic Chemistry; Membrane Fusion; Membranes; Microscopy; Microscopy, Fluorescence; Models, Biological; Nanoparticles - chemistry; Oleic Acid - chemistry; Oligoribonucleotides - chemistry; Organic Chemistry; Peptide Fragments - chemistry; Peptides; Physical Chemistry; Polyelectrolytes; Polyethylenes - chemistry; Prebiotics; Quaternary Ammonium Compounds - chemistry; Ribonucleic acid; RNA
• ISSN: 1755-4330; 1755-4349
• DOI: 10.1038/nchem.1921

Mechanisms of prebiotic compartmentalization are central to providing insights into how protocellular systems emerged on the early Earth. Protocell models are based predominantly on the membrane self-assembly of fatty-acid vesicles, although membrane-free scenarios that involve liquid–liquid microphase separation (coacervation) have also been considered. Here we integrate these alternative models of prebiotic compartmentalization and develop a hybrid protocell model based on the spontaneous self-assembly of a continuous fatty-acid membrane at the surface of preformed coacervate microdroplets prepared from cationic peptides/polyelectrolytes and adenosine triphosphate or oligo/polyribonucleotides. We show that the coacervate-supported membrane is multilamellar, and mediates the selective uptake or exclusion of small and large molecules. The coacervate interior can be disassembled without loss of membrane integrity, and fusion and growth of the hybrid protocells can be induced under conditions of high ionic strength. Our results highlight how notions of membrane-mediated compartmentalization, chemical enrichment and internalized structuration can be integrated in protocell models via simple chemical and physical processes. A hybrid protocell model is described in which a fatty acid membrane spontaneously assembles on the surface of coacervate microdroplets with molecularly crowded interiors. The membrane-enclosed protocells exhibit uptake and exclusion properties that differ from the uncoated droplets. The internal structure can be disassembled at high ionic strength without loss of membrane integrity. This model may help to reconcile alternative mechanisms of prebiotic compartmentalization.