This article is part of a series on Origin and early evolution of life, edited by Dr Eugene V Koonin.

Research

One ancestor for two codes viewed from the perspective of two complementary modes of tRNA aminoacylation

Andrei S Rodin¹ , Eörs Szathmáry^2,3,4 and Sergei N Rodin^2,5

¹  Human Genetics Center, School of Public Health, University of Texas, Houston, TX 77225, USA

²  Collegium Budapest (Institute for Advanced Study), Szentháromság u. 2, H-1014 Budapest, Hungary

³  Parmenides Center for the Study of Thinking, 14a Kardinal Faulhaber Str., D-80333 München, Germany

⁴  Institute of Biology, Eötvös University, 1c Pázmány Péter sétány, H-1117 Budapest, Hungary

⁵  Theoretical Biology, Department of Molecular Biology, Beckman Research Institute of the City of Hope, Duarte, CA 91010, USA

author email corresponding author email

Biology Direct 2009, 4:4doi:10.1186/1745-6150-4-4

Published:	27 January 2009

Abstract

Background

The genetic code is brought into action by 20 aminoacyl-tRNA synthetases. These enzymes are evenly divided into two classes (I and II) that recognize tRNAs from the minor and major groove sides of the acceptor stem, respectively. We have reported recently that: (1) ribozymic precursors of the synthetases seem to have used the same two sterically mirror modes of tRNA recognition, (2) having these two modes might have helped in preventing erroneous aminoacylation of ancestral tRNAs with complementary anticodons, yet (3) the risk of confusion for the presumably earliest pairs of complementarily encoded amino acids had little to do with anticodons. Accordingly, in this communication we focus on the acceptor stem.

Results

Our main result is the emergence of a palindrome structure for the acceptor stem's common ancestor, reconstructed from the phylogenetic trees of Bacteria, Archaea and Eukarya. In parallel, for pairs of ancestral tRNAs with complementary anticodons, we present updated evidence of concerted complementarity of the second bases in the acceptor stems. These two results suggest that the first pairs of "complementary" amino acids that were engaged in primordial coding, such as Gly and Ala, could have avoided erroneous aminoacylation if and only if the acceptor stems of their adaptors were recognized from the same, major groove, side. The class II protein synthetases then inherited this "primary preference" from isofunctional ribozymes.

Conclusion

Taken together, our results support the hypothesis that the genetic code per se (the one associated with the anticodons) and the operational code of aminoacylation (associated with the acceptor) diverged from a common ancestor that probably began developing before translation. The primordial advantage of linking some amino acids (most likely glycine and alanine) to the ancestral acceptor stem may have been selective retention in a protocell surrounded by a leaky membrane for use in nucleotide and coenzyme synthesis. Such acceptor stems (as cofactors) thus transferred amino acids as groups for biosynthesis. Later, with the advent of an anticodon loop, some amino acids (such as aspartic acid, histidine, arginine) assumed a catalytic role while bound to such extended adaptors, in line with the original coding coenzyme handle (CCH) hypothesis.

Reviewers

This article was reviewed by Rob Knight, Juergen Brosius and Anthony Poole.