Deinococcus glutaminyl-tRNA synthetase is a chimer between proteins from an ancient and the modern pathways of aminoacyl-tRNA formation

Deniziak, Marzanna; Sauter, Claude; Becker, Hubert Dominique; Paulus, Caroline; Giegé, Richard; Kern, Daniel

doi:10.1093/nar/gkl1164

Cited by 35 publications

(43 citation statements)

References 49 publications

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“…42 A YqeY domain appended to the C-terminus of the Deinococcus radiodurans GlnRS is important for the enzyme to productively bind to tRNA Gln . 42 The tail domains in the AdT subunits play a similar role by enabling specific binding to their tRNA substrates. 21,22 Because YqeY is homologous to but more distantly related to GatB and GatE than they are to each other, it serves as an ideal outgroup for the tail domain phylogeny.…”

Section: Ancient Divergence Between Gatb and Gatementioning

confidence: 99%

On the Evolution of the tRNA-Dependent Amidotransferases, GatCAB and GatDE

Sheppard

Söll

2008

Journal of Molecular Biology

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SummaryGlutaminyl-tRNA synthetase and asparaginyl-tRNA synthetase evolved from glutamyl-tRNA synthetase and aspartyl-tRNA synthetase, respectively, after the split in the last universal communal ancestor (LUCA). Glutaminyl-tRNA Gln and asparaginyl-tRNA Asn were likely formed in LUCA by amidation of the mischarged species, glutamyl-tRNA Gln and aspartyl-tRNA Asn , by tRNA-dependent amidotransferases as is still the case in most bacteria and all known archaea. The amidotransferase GatCAB is found in both domains of life while the heterodimeric amidotransferase, GatDE, is found only in Archaea. The GatB and GatE subunits belong to a unique protein family with Pet112 that is encoded in the nuclear genomes of numerous eukaryotes. GatE was thought to have evolved from GatB after the emergence of the modern lines of decent. Our phylogenetic analysis though places the split between GatE and GatB prior to the phylogenetic divide between Bacteria and Archaea and Pet112 to be of mitochondrial origin. In addition, GatD appears to have emerged prior to the bacterialarchaeal phylogenetic divide. Thus, while GatDE is an archaeal signature protein it likely was present in LUCA together with GatCAB. Archaea retained both amidotransferases while Bacteria emerged with only GatCAB. The presence of GatDE has favored a unique archaeal tRNA Gln that may be preventing acquisition of glutaminyl-tRNA synthetase in Archaea. Archaeal GatCAB on the other hand has not favored a distinct tRNA Asn suggesting tRNA Asn recognition is not a major barrier to the retention of asparaginyl-tRNA synthetase in more Archaea.

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Section: Ancient Divergence Between Gatb and Gatementioning

confidence: 99%

On the Evolution of the tRNA-Dependent Amidotransferases, GatCAB and GatDE

Sheppard

Söll

2008

Journal of Molecular Biology

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“…These recognition complexes effect the transfer of activated amino acids to the correct tRNA molecule, producing aminoacyl-tRNAs needed for protein synthesis by the ribosome. Errors in charging are rare (3,4), and it is generally agreed that the low frequency of mischarging is based on synthetase recognition of specific identity elements in tRNA molecules (5). Many investigators (6)(7)(8) have observed that the codon table tends to reduce deleterious effects of point mutations (9) by assuring that they do minimal violence to the physical requirements of protein folding.…”

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confidence: 99%

tRNA acceptor stem and anticodon bases form independent codes related to protein folding

Carter

Wolfenden

2015

Proc. Natl. Acad. Sci. U.S.A.

123

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Aminoacyl-tRNA synthetases recognize tRNA anticodon and 3′ acceptor stem bases. Synthetase Urzymes acylate cognate tRNAs even without anticodon-binding domains, in keeping with the possibility that acceptor stem recognition preceded anticodon recognition. Representing tRNA identity elements with two bits per base, we show that the anticodon encodes the hydrophobicity of each amino acid side-chain as represented by its water-to-cyclohexane distribution coefficient, and this relationship holds true over the entire temperature range of liquid water. The acceptor stem codes preferentially for the surface area or size of each sidechain, as represented by its vapor-to-cyclohexane distribution coefficient. These orthogonal experimental properties are both necessary to account satisfactorily for the exposed surface area of amino acids in folded proteins. Moreover, the acceptor stem codes correctly for β-branched and carboxylic acid side-chains, whereas the anticodon codes for a wider range of such properties, but not for size or β-branching. These and other results suggest that genetic coding of 3D protein structures evolved in distinct stages, based initially on the size of the amino acid and later on its compatibility with globular folding in water.genetic code | aminoacyl-tRNA synthetases | urzymes | multivariate regression | protein folding T he genetic code is implemented by two distinct superfamilies of protein-RNA complexes between an aminoacyl-tRNA synthetase (aaRS) from one of two classes (1, 2) and its cognate tRNA. These recognition complexes effect the transfer of activated amino acids to the correct tRNA molecule, producing aminoacyl-tRNAs needed for protein synthesis by the ribosome. Errors in charging are rare (3, 4), and it is generally agreed that the low frequency of mischarging is based on synthetase recognition of specific identity elements in tRNA molecules (5). Many investigators (6-8) have observed that the codon table tends to reduce deleterious effects of point mutations (9) by assuring that they do minimal violence to the physical requirements of protein folding. One earlier study (10) identified a nonrandom tendency for hydrophilic side-chains to be coded by an A as the second codon base, hinting at more extensive relationships between the code and factors that direct protein folding.tRNA identity elements (5, 11) map to both the anticodon and acceptor stem at opposite ends of the L-shaped tRNA molecule and are distinct from binding determinants for elongation factorTu in the T-stem (12). Invariant cores of both classes of aaRS, termed urzymes (from the prefix ur-= primitive), lack anticodon-binding domains and cannot recognize the anticodon. However, they catalyze amino acid activation and acyl transfer with K M values approaching those of contemporary aaRS, consistent with their participation in early protein synthesis (13-16). The implied ability of ancestral aaRS to recognize tRNA acceptor stems, but not anticodons, is consistent with the suggestion that the earliest proteins were coded no...

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“…A similar model has recently been proposed for a natural chimeric synthetase, the Deinococcus GlnRS. 26 This enzyme contains a unique C-terminal extension, which is a paralog of the Yqey proteins and increases the affinity of the enzyme for its cognate tRNA. As the TRBD present in aminoacyl-tRNA synthetases and non-catalytic proteins, Yqey proteins exist either in free form or as appendices to GlnRSs and the tRNA-binding subunits of bacterial and archaeal amidotransferases.…”

Section: Discussionmentioning

confidence: 99%