Genome Evolution from Random Ligation of RNAs of Autocatalytic Sets

Abstract

The evolutionary origin of the genome remains elusive. Here, I hypothesize that its first iteration, the protogenome, was a multi-ribozyme RNA. It evolved, likely within liposomes (the protocells) forming in dry-wet cycling environments, through the random fusion of ribozymes by a ligase and was amplified by a polymerase. The protogenome thereby linked, in one molecule, the information required to seed the protometabolism (a combination of RNA-based autocatalytic sets) in newly forming protocells. If this combination of autocatalytic sets was evolutionarily advantageous, the protogenome would have amplified in a population of multiplying protocells. It likely was a quasispecies with redundant information, e.g., multiple copies of one ribozyme. As such, new functionalities could evolve, including a genetic code. Once one or more components of the protometabolism were templated by the protogenome (e.g., when a ribozyme was replaced by a protein enzyme), and/or addiction modules evolved, the protometabolism became dependent on the protogenome. Along with increasing fidelity of the RNA polymerase, the protogenome could grow, e.g., by incorporating additional ribozyme domains. Finally, the protogenome could have evolved into a DNA genome with increased stability and storage capacity. I will provide suggestions for experiments to test some aspects of this hypothesis.

Abiogenesis through gradual evolution of autocatalysis into template‐based replication

“…In contrast to scenarios postulating that evolution began with the sudden appearance of a self‐replicase, we propose more gradual routes for the emergence of evolution [140–142], starting from collective autocatalysis, then its coupling with template‐based ligation, and finally the advent of template‐based replication. We first describe possible gradual paths and then discuss the functional and molecular continuities and discontinuities that are encountered along the way, highlighting the role of compartmentalisation in scaffolding intermediate regimes.…”