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, such as evaluating the ability of ribozyme RNA polymerases to generate random ligation products and testing the catalytic activity of linked ribozyme domains.

Self-empowerment of life through RNA networks, cells and viruses

“…, a new capability to generate and test innovative tools of adaptation ( Marshall & Bredy, 2016 ; Mattick, 2010 ; Frías-Lasserre & Villagra, 2017 ; Stajic & Jansen, 2021 ). This new capability enables organisms to better adapt to environmental circumstances, with various behavioral patterns such as escape, invent, recombine, exapt, coopt, suppress, displace, compete and cooperate and their transgenerational inheritance ( Jablonka, 2013 ; Broecker, 2021 ).…”

Biological Catalysis and Information Storage Have Relied on N-Glycosyl Derivatives of β-D-Ribofuranose since the Origins of Life

“…Combining the results of these seemingly distant studies yields a coherent picture that can logically reflect the origins and subsequent evolution of life on Earth. It is now believed that the hydrothermal vents or geothermal fields on the sea or ocean floor provided an adequate environment for life on Earth to start, due to the availability of chemicals that would have been necessary to sustain the metabolic processes of the time [12][13][14][15][16][17][18][19][20]. Were these primary forms of life based on the transfer of information via the DNA -> RNA -> protein pathway, as life forms are today?…”

“…The fusion of the "RNA-based World" and the "lipid world", including the encapsulation of self-replicating RNA (ribozymes) into cellular-type lipid systems (e.g., liposomes), which took place either simultaneously or sometime later, could have marked the occurrence of primary life on Earth [15][16][17][71][72][73]. The compartmentalization of a so-called autocatalytic set containing catalytically active RNAs, possibly with other organic compounds (e.g., peptides, cofactors, etc.)…”

“…The compartmentalization of a so-called autocatalytic set containing catalytically active RNAs, possibly with other organic compounds (e.g., peptides, cofactors, etc.) ensured the self-replication process(es) to be sustainable and capable of evolution [17,74]. The diffusion processes, as well as micromolar concentrations of organic compounds in an oceanic environment, would otherwise prevent the self-replication of the system [15,28].…”

“…As the RNA molecules evolved over time, new features began to emerge, which enabled increasingly complex metabolism controlled by a ribozyme-based catalysis [1,17,[90][91][92][93]. Owing to their capacity for the selective binding of nucleotide-derived cofactors (coribozymes), amino acids and peptides, substrates and environmental cations, in particular, metal cations such as Mg 2+ , Mn 2+ , Co 2+ or Fe 2+ [94][95][96], the range of reactions catalyzed by RNA molecules was broadened to include redox processes, as well as the transfer of electrons and simple functional groups.…”