Non-enzymatic oligonucleotide ligation in coacervate protocells sustains compartment-content coupling

Tommaso P. Fraccia () and Nicolas Martin ()
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Tommaso P. Fraccia: Institut Pierre-Gilles de Gennes, Chimie Biologie et Innovation, UMR 8231, ESPCI Paris, PSL University, CNRS
Nicolas Martin: Univ. Bordeaux, CNRS, Centre de Recherche Paul Pascal, UMR 5031

Nature Communications, 2023, vol. 14, issue 1, 1-12

Abstract: Abstract Modern cells are complex chemical compartments tightly regulated by an underlying DNA-encoded program. Achieving a form of coupling between molecular content, chemical reactions, and chassis in synthetic compartments represents a key step to the assembly of evolvable protocells but remains challenging. Here, we design coacervate droplets that promote non-enzymatic oligonucleotide polymerization and that restructure as a result of the reaction dynamics. More specifically, we rationally exploit complexation between end-reactive oligonucleotides able to stack into long physical polymers and a cationic azobenzene photoswitch to produce three different phases—soft solids, liquid crystalline or isotropic coacervates droplets—each of them having a different impact on the reaction efficiency. Dynamical modulation of coacervate assembly and dissolution via trans-cis azobenzene photo-isomerization is used to demonstrate cycles of light-actuated oligonucleotide ligation. Remarkably, changes in the population of polynucleotides during polymerization induce phase transitions due to length-based DNA self-sorting to produce multiphase coacervates. Overall, by combining a tight reaction-structure coupling and environmental responsiveness, our reactive coacervates provide a general route to the non-enzymatic synthesis of polynucleotides and pave the way to the emergence of a primitive compartment-content coupling in membrane-free protocells.

Date: 2023
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DOI: 10.1038/s41467-023-38163-8

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