Spontaneous Recombination of Short RNAs to Increase Length and Complexity in Prebiotically Plausible Conditions

The RNA World hypothesis is an influential theory of how life arose on earth which posits that the earliest life forms carried out essential activities with RNA catalysts instead of proteins. Substantial evidence to support this theory comes from among others, the fact that the ribosome is a ribozyme, the existence of small RNA catalysts capable of high activity, and self-assembling ribozymes such as the Azoarcus ribozyme. Additional support has been provided by the directed evolution of various ribozymes and the reputed prebiotic synthesis of nucleotides and small RNA oligomers. However, it has long been challenging to show how long RNA catalysts could have emerged from prebiotic syntheses or be formed by nonenzymatic processes. Here, I suggest that energetically neutral RNA-RNA recombinations could have created longer oligomers from short precursors generated from nonenzymatic prebiotic syntheses. I show that small RNAs less than 20 nucleotides long are capable of recombination by up to three unique mechanisms and confirm that the activity is intrinsic to the RNA. I further show that the reaction profile changes under different conditions, including pH and magnesium concentration, and that some products may have distinctly different structures. Finally, I show that the reaction improves with time and can be reproduced with similar RNAs according to sequence or structure. These results demonstrate that RNA-RNA recombination is an inherently plausible means of diversification, elongation, and enhancement for small, abiotically generated oligomers, and indicate that a capacity for spontaneous RNA-RNA recombination is a fundamental property of all RNA molecules.