The ability to process molecules available in the environment into useable building blocks characterizes catabolism in contemporary cells and was probably critical for the initiation of life. Here we show that a catabolic process in collectively autocatalytic sets of RNAs allows diversified substrates to be assimilated. We modify fragments of the Azoarcus group I intron and find that the system is able to restore the original native fragments by a multi-step reaction pathway. This allows in turn the formation of catalysts by an anabolic process, eventually leading to the accumulation of ribozymes. These results demonstrate that rudimentary self-reproducing RNA systems based on recombination possess an inherent capacity to assimilate an expanded repertoire of chemical resources and suggest that coupled catabolism and anabolism could have arisen at a very early stage in primordial living systems.
33Evolution via template-based replication 1-4 was probably preceded by a more rudimentary form 34 of evolution based on networks of autocatalytic reactions [5][6][7][8] . However, reaction networks 35 possessing the Darwinian properties of variation (in composition, the catalysts present and their 36 relative amounts), differential reproduction (accumulation of products), and heredity 37 (persistence of composition), have so far not been identified. Here we show that networks of 38 catalytic RNAs can possess certain properties of Darwinian systems, that these properties are 39 controlled by network topology, and characterize important trade-offs between them. By 40 combining barcoded sequencing with droplet microfluidics, we screened ̴ 20,000 reactions 41 corresponding to more than 1,800 distinct networks of ribozymes that catalyse their own 42 formation from RNA fragments. We found that more highly connected networks tend to 43 reproduce more quickly (accumulate more ribozymes) and be more robust to perturbations, 44 indicating a trade-off between variation and reproduction. Variations are strongest when adding 45 upstream ribozymes with novel reaction specificities (innovations) which target weakly 46 connected networks. In turn, innovations increase connectivity, thus buffer against further 47 Main 59In the prebiotic world, the spontaneous appearance of an RNA polymerase ribozyme (a 60 replicase) with sufficient processivity to allow self-replication and enough fidelity to avoid an 61 error catastrophe 5,6 seems unlikely, given that known replicases are long (>165 nt) and 62 structurally complex 1-4 . However, theoretical studies suggest that earlier modes of evolution 63 could have been supported by autocatalytic sets, where reproduction results from networks of 64 more rudimentary catalysts [11][12][13] . Consistently, recent experiments indicate that RNA 65 polymerase ribozymes can assemble from catalytic networks of RNA oligomers 14 , suggesting 66 that replicases may have emerged as components of such networks. Nevertheless, sustaining 67 evolution in reaction networks is by no means trivial, as the Darwinian properties of variation, 68 heredity and selection are mediated by chemical compositions (the proportion of different 69 chemical species) rather than the copying of a sequence. Furthermore, the possibility to evolve 70 chemistries may be constained by trade-offs between these properties. For instance, robustness 71 to environmental perturbations and persistence of compositions are necessary for selection to 72 act, but must be balanced with variation to explore novel states. So far, none of these Darwinian 73properties, nor their interplay, have been experimentally studied at a large scale in a 74 prebiotically relevant system. 75We studied an experimental model of autocatalytic RNAs derived from the group I intron of 76 the Azoarcus bacterium 15 . Fragments (denoted WXY and Z) assemble into non-covalent 77 complexes that catalyze the formation of more efficient covalent ribozymes 16,17 (denoted 78...
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