Abstract

Self-replicating molecules, in particular RNA, have long been assumed as key to origins of life on Earth. This notion, however, is not very secure since the reduction of life's complexity to self-replication alone relies on thermodynamically untenable assumptions. Alternative, earlier hypotheses about peptide-dominated colloid self-assembly should be revived. Such macromolecular conglomerates presumably existed in a dynamic equilibrium between confluent growth in sessile films and microspheres detached in turbulent suspension. The first organic syntheses may have been driven by mineral-assisted photoactivation at terrestrial geothermal fields, allowing photo-dependent heterotrophic origins of life. Inherently endowed with rudimentary catalyst activities, mineral-associated organic microstructures can have evolved adaptively toward cooperative 'protolife' communities, in which 'protoplasmic continuity' was maintained throughout a graded series of 'proto-biofilms', 'protoorganisms' and 'protocells' toward modern life. The proneness of organic microspheres to merge back into the bulk of sessile films by spontaneous fusion can have made large populations promiscuous from the beginning, which was important for the speed of collective evolution early on. In this protein-centered scenario, the emergent coevolution of uncoded peptides, metabolic cofactors and oligoribonucleotides was primarily optimized for system-supporting catalytic capabilities arising from nonribosomal peptide synthesis and nonreplicative ribonucleotide polymerization, which in turn incorporated other reactive micromolecular organics as vitamins and cofactors into composite macromolecular colloid films and microspheres. Template-dependent replication and gene-encoded protein synthesis emerged as secondary means for further optimization of overall efficieny later on. Eventually, Darwinian speciation of cell-like lineages commenced after minimal gene sets had been bundled in transmissible genomes from multigenomic protoorganisms.

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