Journal
MOLECULAR BIOLOGY AND EVOLUTION
Volume 34, Issue 5, Pages 1252-1260Publisher
OXFORD UNIV PRESS
DOI: 10.1093/molbev/msx086
Keywords
protein evolution; ribosomal protein; origin of life; ribosomal origins and evolution; origins of protein folding; beta-harpin
Funding
- NASA [NNX16AJ29G]
- NASA [NNX16AJ29G, 902612] Funding Source: Federal RePORTER
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The ribosome is imprinted with a detailed molecular chronology of the origins and early evolution of proteins. Here we show that when arranged by evolutionary phase of ribosomal evolution, ribosomal protein (rProtein) segments reveal an atomic level history of protein folding. The data support a model in which aboriginal oligomers evolved into globular proteins in a hierarchical step-wise process. Complexity of assembly and folding of polypeptide increased incrementally in concert with expansion of rRNA. (i) Short random coil proto-peptides bound to rRNA, and (ii) lengthened over time and coalesced into beta-beta secondary elements. These secondary elements (iii) accreted and collapsed, primarily into beta-domains. Domains (iv) accumulated and gained complex super-secondary structures composed of mixtures of alpha-helices and beta-strands. Early protein evolution was guided and accelerated by interactions with rRNA. rRNA and proto-peptide provided mutual protection from chemical degradation and disassembly. rRNA stabilized polypeptide assemblies, which evolved in a stepwise process into globular domains, bypassing the immense space of random unproductive sequences. Coded proteins originated as oligomers and polymers created by the ribosome, on the ribosome and for the ribosome. Synthesis of increasingly longer products was iteratively coupled with lengthening and maturation of the ribosomal exit tunnel. Protein catalysis appears to be a late byproduct of selection for sophisticated and finely controlled assembly.
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