Ancestral AlaX editing enzymes for control of genetic code fidelity are not tRNA-specific

J Biol Chem. 2015 Apr 17;290(16):10495-503. doi: 10.1074/jbc.M115.640060. Epub 2015 Feb 27.

Abstract

Accurate protein synthesis requires the hydrolytic editing of tRNAs incorrectly aminoacylated by aminoacyl-tRNA synthetases (ARSs). Recognition of cognate tRNAs by ARS is less error-prone than amino acid recognition, and, consequently, editing domains are generally believed to act only on the tRNAs cognate to their related ARSs. For example, the AlaX family of editing domains, including the editing domain of alanyl-tRNA synthetase and the related free-standing trans-editing AlaX enzymes, are thought to specifically act on tRNA(Ala), whereas the editing domains of threonyl-tRNA synthetases are specific for tRNA(Thr). Here we show that, contrary to this belief, AlaX-S, the smallest of the extant AlaX enzymes, deacylates Ser-tRNA(Thr) in addition to Ser-tRNA(Ala) and that a single residue is important to determine this behavior. Our data indicate that promiscuous forms of AlaX are ancestral to tRNA-specific AlaXs. We propose that former AlaX domains were used to maintain translational fidelity in earlier stages of genetic code evolution when mis-serylation of several tRNAs was possible.

Keywords: AlaX; Aminoacyl tRNA Synthetase; Genetic Code; Mistranslation; Proofreading; Protein Evolution; RNA Editing; phylogenetics; tRNA.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Amino Acyl-tRNA Synthetases / chemistry
  • Amino Acyl-tRNA Synthetases / genetics
  • Amino Acyl-tRNA Synthetases / metabolism*
  • Archaeal Proteins / chemistry
  • Archaeal Proteins / genetics
  • Archaeal Proteins / metabolism*
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Evolution, Molecular
  • Genetic Code*
  • Models, Molecular
  • Molecular Sequence Data
  • Nucleic Acid Conformation
  • Phylogeny
  • Protein Biosynthesis
  • Protein Structure, Tertiary
  • Pyrococcus abyssi / classification
  • Pyrococcus abyssi / genetics
  • Pyrococcus abyssi / metabolism*
  • Pyrococcus horikoshii / classification
  • Pyrococcus horikoshii / genetics
  • Pyrococcus horikoshii / metabolism*
  • RNA Editing
  • RNA, Transfer / chemistry
  • RNA, Transfer / genetics
  • RNA, Transfer / metabolism*
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Sequence Alignment

Substances

  • Archaeal Proteins
  • Recombinant Proteins
  • RNA, Transfer
  • Amino Acyl-tRNA Synthetases