Divergence of glutamate and glutamine aminoacylation pathways: providing the evolutionary rationale for mischarging.
Aminoacyl-tRNA for protein synthesis is produced through the action of a family of enzymes called aminoacyl-tRNA synthetases. A general rule is that there is one aminoacyl-tRNA synthetase for each of the standard 20 amino acids found in all cells. This is not universal, however, as a majority of prokaryotic organisms and eukaryotic organelles lack the enzyme glutaminyl-tRNA synthetase, which is responsible for forming Gln-tRNAGln in eukaryotes and in Gram-negative eubacteria. Instead, in organisms lacking glutaminyl-tRNA synthetase, Gln-tRNAGln is provided by misacylation of tRNAGln with glutamate by glutamyl-tRNA synthetase, followed by the conversion of tRNA-bound glutamate to glutamine by the enzyme Glu-tRNAGln amidotransferase. The fact that two different pathways exist for charging glutamine tRNA indicates that ancestral prokaryotic and eukaryotic organisms evolved different cellular mechanisms for incorporating glutamine into proteins. Here, we explore the basis for diverging pathways for aminoacylation of glutamine tRNA. We propose that stable retention of glutaminyl-tRNA synthetase in prokaryotic organisms following a horizontal gene transfer event from eukaryotic organisms (Lamour et al. 1994) was dependent on the evolving pool of glutamate and glutamine tRNAs in the organisms that acquired glutaminyl-tRNA synthetase by this mechanism. This model also addresses several unusual aspects of aminoacylation by glutamyl- and glutaminyl-tRNA synthetases that have been observed.
Rogers
K C
KC
Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06520-8114, USA.
Söll
D
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D000215:Acylation; D000604:Amino Acyl-tRNA Synthetases / Q000378:metabolism*; D000926:Anticodon; D005075:Biological Evolution; D005057:Eukaryotic Cells / Q000201:enzymology; D005815:Genetic Code; D005975:Glutamate-tRNA Ligase / Q000378:metabolism*; D018698:Glutamic Acid / Q000378:metabolism*; D005973:Glutamine / Q000378:metabolism*; D008957:Models, Genetic; D019884:Nitrogenous Group Transferases; D011387:Prokaryotic Cells / Q000201:enzymology; D012346:RNA, Transfer, Amino Acyl / Q000096:biosynthesis*; D012351:RNA, Transfer, Gln / Q000378:metabolism; D012352:RNA, Transfer, Glu / Q000378:metabolism; D014166:Transferases / Q000378:metabolism*
D000926:Anticodon; D012346:RNA, Transfer, Amino Acyl; D012351:RNA, Transfer, Gln; D012352:RNA, Transfer, Glu; D005973:Glutamine; D018698:Glutamic Acid; D014166:Transferases; D019884:Nitrogenous Group Transferases; C047694:glutamyl-tRNA(Gln) amidotransferase; D000604:Amino Acyl-tRNA Synthetases; D005975:Glutamate-tRNA Ligase; C020659:glutaminyl-tRNA synthetase