Abstract
It was Francis Crick who first asked why the ribosome contains so much RNA, and discussed the implications of this for the direct flow of genetic information from DNA to protein. Remarkable advances in our understanding of the ribosome and protein synthesis, including the recent publication of two mammalian mitochondrial ribosome structures, have shed new light on this intriguing aspect of evolution in molecular biology. We examine here whether RNA is indispensable for coded protein synthesis, or whether an all-protein ‘ribosome’ (or ‘synthosome’) might be possible, with a protein enzyme catalyzing peptide synthesis, and release factor-like protein adaptors able to read a message composed of deoxyribonucleotides. We also compare the RNA world hypothesis with the alternative ‘proteins first’ hypothesis in terms of their different understandings of the evolution of the ribosome, and whether this might have been preceded by an ancestral form of nonribosomal peptide synthesis catalyzed by protein enzymes.
Highlights
A Ribosome Without RNAIt was Francis Crick who first asked why the ribosome contains so much RNA, and discussed the implications of this for the flow of genetic information from DNA to protein
The RNA world hypothesis—that RNA once functioned as the principal biological catalyst and informational storage molecule—proposes that many of the roles played by RNA in modern biochemistry are leftover relics of this ancient period (Atkins et al, 2011; Bernhardt, 2012), with its ancestral enzymatic activities mainly superseded by protein catalysts with higher catalytic efficiencies (Doudna and Lorsch, 2005; but see Jeffares et al, 1998 and further discussion below), and its informational role largely assumed by DNA, with the latter’s greater chemical stability at neutral pH (Ferris and Usher, 1983)
Despite the molecular complexity that is provided by DNA and protein, RNA remains essential for information flow from DNA to protein in contemporary molecular biology
Summary
It was Francis Crick who first asked why the ribosome contains so much RNA, and discussed the implications of this for the flow of genetic information from DNA to protein. Remarkable advances in our understanding of the ribosome and protein synthesis, including the recent publication of two mammalian mitochondrial ribosome structures, have shed new light on this intriguing aspect of evolution in molecular biology. We examine here whether RNA is indispensable for coded protein synthesis, or whether an all-protein “ribosome” (or “synthosome”) might be possible, with a protein enzyme catalyzing peptide synthesis, and release factor-like protein adaptors able to read a message composed of deoxyribonucleotides. We compare the RNA world hypothesis with the alternative “proteins first” hypothesis in terms of their different understandings of the evolution of the ribosome, whether ribosomal protein synthesis carried out by RNA might have been preceded by an ancestral form of nonribosomal peptide synthesis carried out by protein enzymes. Specialty section: This article was submitted to Evolutionary and Genomic Microbiology, a section of the journal Frontiers in Ecology and Evolution
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