Darwinian Evolution of Self-Replicating DNA in a Synthetic Protocell

Zhanar Abil, Ana María Restrepo Sierra, Andreea R. Stan, Amélie Châne, Alicia Prado, Miguel Vega, Yannick Rondelez and Christophe Danelon ()
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Zhanar Abil: Delft University of Technology
Ana María Restrepo Sierra: Delft University of Technology
Andreea R. Stan: Delft University of Technology
Amélie Châne: Delft University of Technology
Alicia Prado: 1
Miguel Vega: 1
Yannick Rondelez: 10 rue Vauquelin
Christophe Danelon: Delft University of Technology

Nature Communications, 2024, vol. 15, issue 1, 1-15

Abstract: Abstract Replication, heredity, and evolution are characteristic of Life. We and others have postulated that the reconstruction of a synthetic living system in the laboratory will be contingent on the development of a genetic self-replicator capable of undergoing Darwinian evolution. Although DNA-based life dominates, the in vitro reconstitution of an evolving DNA self-replicator has remained challenging. We hereby emulate in liposome compartments the principles according to which life propagates information and evolves. Using two different experimental configurations supporting intermittent or semi-continuous evolution (i.e., with or without DNA extraction, PCR, and re-encapsulation), we demonstrate sustainable replication of a linear DNA template – encoding the DNA polymerase and terminal protein from the Phi29 bacteriophage – expressed in the ‘protein synthesis using recombinant elements’ (PURE) system. The self-replicator can survive across multiple rounds of replication-coupled transcription-translation reactions in liposomes and, within only ten evolution rounds, accumulates mutations conferring a selection advantage. Combined data from next-generation sequencing with reverse engineering of some of the enriched mutations reveal nontrivial and context-dependent effects of the introduced mutations. The present results are foundational to build up genetic complexity in an evolving synthetic cell, as well as to study evolutionary processes in a minimal cell-free system.

Date: 2024
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DOI: 10.1038/s41467-024-53226-0

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