Revisiting the Extinction of the RNA World

Abstract

The ribozyme world is thought to have evolved the burdensome complexity of peptide and protein synthesis because the 20 amino acid side chains are catalytically superior. Instead, I propose that the Achilles heel of the RNA world that led to the extinction of riboorganisms was RNA's polyanionic charges that could not be covalently neutralized stably by phosphotriester formation. These charges prevented development of hydrophobic cores essential for integration into membranes and many enzymatic reactions. In contrast, the phosphotriester modification of DNA is stable. So, the fact that the charge was never removed in DNA evolution gives further credence to proteins coming before DNA.

Figure 1

Evolution of RNA to encode polymers containing hydrophobic cores. Two easy evolutionary roads to hydrophobic cores were not taken by RNA (two arrows to red X) because the removal of the negative charge shown leads to rearrangement. Rearrangement is inhibited in DNA by its 2′ H, yet DNA also did not lose charges, giving further credence to protein evolving first (left green arrow).

Figure 2

Evolution of protein synthesis. The proposed pathway from amino acids to proteins (green) is based on RNAs (red). Identifiable descendants of aminoacyl-tRNA synthetase ribozymes are extinct, and the ancestral function of the ribosomal small subunit ribozyme is a mystery. Although this pathway is necessarily very complex and speculative, many^, of the pathways proposed in the literature are similar. A quite different alternative is evolution from an RNA helicase.