The Rodin-Ohno hypothesis that two enzyme superfamilies descended from one ancestral gene: an unlikely scenario for the origins of translation that will not be dismissed

Biology Direct

Charles W Carter¹  Li Li¹  Violetta Weinreb¹  Martha Collier¹  Katiria Gonzalez-Rivera¹  Mariel Jimenez-Rodriguez¹  Ozgün Erdogan¹  Brian Kuhlman¹  Xavier Ambroggio²  Tishan Williams¹  S Niranj Chandrasekharan¹ 

[1] Department of Biochemistry and Biophysics, CB 7260 University of North Carolina at Chapel Hill, Chapel Hill, NC 27599-7260, USA

[2] Present address: Rosetta Design Group LLC, 47 Maple Street Suite 202, Burlington, VT 05401, USA

关键词: Sense/antisense coding;    Ancestral genes;    Structural homology;    Amino acid activation;    RNA World hypothesis;    Origin of Translation;    Genetic code;    Urzymes;    Aminoacyl-tRNA synthetases;   

Others  :  799732
DOI  :  10.1186/1745-6150-9-11

 received in 2014-03-25, accepted in 2014-05-19,  发布年份 2014

【 摘 要 】

Background

Because amino acid activation is rate-limiting for uncatalyzed protein synthesis, it is a key puzzle in understanding the origin of the genetic code. Two unrelated classes (I and II) of contemporary aminoacyl-tRNA synthetases (aaRS) now translate the code. Observing that codons for the most highly conserved, Class I catalytic peptides, when read in the reverse direction, are very nearly anticodons for Class II defining catalytic peptides, Rodin and Ohno proposed that the two superfamilies descended from opposite strands of the same ancestral gene. This unusual hypothesis languished for a decade, perhaps because it appeared to be unfalsifiable.

Results

The proposed sense/antisense alignment makes important predictions. Fragments that align in antiparallel orientations, and contain the respective active sites, should catalyze the same two reactions catalyzed by contemporary synthetases. Recent experiments confirmed that prediction. Invariant cores from both classes, called Urzymes after Ur = primitive, authentic, plus enzyme and representing ~20% of the contemporary structures, can be expressed and exhibit high, proportionate rate accelerations for both amino-acid activation and tRNA acylation. A major fraction (60%) of the catalytic rate acceleration by contemporary synthetases resides in segments that align sense/antisense. Bioinformatic evidence for sense/antisense ancestry extends to codons specifying the invariant secondary and tertiary structures outside the active sites of the two synthetase classes. Peptides from a designed, 46-residue gene constrained by Rosetta to encode Class I and II ATP binding sites with fully complementary sequences both accelerate amino acid activation by ATP ~400 fold.

Conclusions

Biochemical and bioinformatic results substantially enhance the posterior probability that ancestors of the two synthetase classes arose from opposite strands of the same ancestral gene. The remarkable acceleration by short peptides of the rate-limiting step in uncatalyzed protein synthesis, together with the synergy of synthetase Urzymes and their cognate tRNAs, introduce a new paradigm for the origin of protein catalysts, emphasize the potential relevance of an operational RNA code embedded in the tRNA acceptor stems, and challenge the RNA-World hypothesis.

Reviewers

This article was reviewed by Dr. Paul Schimmel (nominated by Laura Landweber), Dr. Eugene Koonin and Professor David Ardell.

【 授权许可】

   
2014 Carter et al.; licensee BioMed Central Ltd.

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