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The emergence of replicases that can replicate themselves is a central issuein the origin of life. Recent experiments suggest that such replicases can berealized if an RNA polymerase ribozyme is divided into fragments short enoughto be replicable by the ribozyme and if these fragments self-assemble into afunctional ribozyme. However, the continued self-replication of such replicasesrequires that the production of every essential fragment be balanced andsustained. Here, we use mathematical modeling to investigate whether and underwhat conditions fragmented replicases achieve continued self-replication. Wefirst show that under a simple batch condition, the replicases fail to displaycontinued self-replication owing to positive feedback inherent in thesereplicases. This positive feedback inevitably biases replication toward asubset of fragments, so that the replicases eventually fail to sustain theproduction of all essential fragments. We then show that this inherentinstability can be resolved by small rates of random content exchange betweenloose compartments (i.e., horizontal transfer). In this case, the balancedproduction of all fragments is achieved through negative frequency-dependentselection operating in the population dynamics of compartments. This selectionmechanism arises from an interaction mediated by horizontal transfer betweenintracellular and intercellular symmetry breaking. The horizontal transfer alsoensures the presence of all essential fragments in each compartment, sustainingself-replication. Taken together, our results underline compartmentalizationand horizontal transfer in the origin of the first self-replicating replicases.

Horizontal transfer between loose compartments stabilizes replication of fragmented ribozymes