Mechanism of tRNA recognition by heterotetrameric glycyl-tRNA synthetase from lactic acid bacteria

Nagato, Yasuha; Yamashita, Seisuke; Ohashi, Akiyoshi; Furukawa, Haruyuki; Takai, Kazuyuki; Tomita, Kozo; Tomikawa, Chie

doi:10.1093/jb/mvad043

Cited by 3 publications

(2 citation statements)

References 47 publications

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“…The signatures of tRNA Ala are G2:C71, G3:U70, C4:G69, and A73. In uniAlaRS, the wobble base pair G3:U70 is the main identity determinant for tRNA Ala aminoacylation by uniAlaRS (40; 33; 37; 41; 42; 34). The ATL domain interacts with the base of the discriminator position (U73 in tRNA Gly , and A73 in tRNA Ala ).…”

Section: Resultsmentioning

confidence: 99%

Common evolutionary origins of the bacterial glycyl tRNA synthetase and alanyl tRNA synthetase

Álvarez-Carreño

Arciniega

Pouplana

et al. 2023

Preprint

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Glycyl tRNA aminoacylation is catalyzed by different enzymes in different lineages of the Tree of Life. The archaeal (arcGlyRS) and bacterial (bacGlyRS) versions of glycyl tRNA synthetase are globally different. arcGlyRS is a relatively small protein with two domains: a catalytic domain and a tRNA recognition domain. bacGlyRS is a large, multi-domain protein. We have investigated the complex evolutionary histories of these enzymes. Component domains of bacGlyRS show common ancestry with 1) the catalytic domain of class II tRNA synthetases; 2) the HD domain of the bacterial RNase Y; 3) the body and tail domains of the archaeal CCA-adding enzyme; 5) the anti-codon binding domain of the arginyl tRNA synthetase; and a previously unrecognized domain that we call ATL (Ancient tRNA linkup). The emergence of bacGlyRS in its extant form would have required the recruitment of domains from a pool of existing homologs, possibly at different times, by a process of molecular bricolage. A domain-by-domain analysis reveals that the catalytic and ATL domains are closely related to domains in the universal alanyl tRNA synthetase. Homology of the HD domain to bacteria-specific proteins and homology of the body and tail domains to the archaeal CCA-adding enzyme suggest a later recruitment. The data suggest that bacGlyRS was present at the last bacterial common ancestor and that bacGlyRS and uniAlaRS emerged from a shared core before the last common universal ancestor, suggesting that bacGlyRS and uniAlaRS evolved by a stepwise accumulation of protein domains during the dawn of biology.

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Section: Resultsmentioning

confidence: 99%

Common evolutionary origins of the bacterial glycyl tRNA synthetase and alanyl tRNA synthetase

Álvarez-Carreño

Arciniega

Pouplana

et al. 2023

Preprint

View full text Add to dashboard Cite

show abstract

“…The signatures of tRNA Ala are G2:C71, G3:U70, C4: G69, and A73. In uniAlaRS, the wobble base pair G3:U70 is the main identity determinant for tRNA Ala aminoacylation by uniAlaRS (Chong et al, 2018;McClain et al, 1991;Naganuma et al, 2009Naganuma et al, , 2014Nagato et al, 2023;Yu et al, 2023). The ATL domain interacts with the base of the discriminator position (U73 in tRNA Gly , and A73 in tRNA Ala ).…”

Section: Bacglyrs and Unialars Homology Is Observed In Key Functional...mentioning

confidence: 99%

Common evolutionary origins of the bacterial glycyl tRNA synthetase and alanyl tRNA synthetase

Alvarez‐Carreño,

Arciniega,

Ribas de Pouplana

et al. 2024

Protein Science

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Aminoacyl‐tRNA synthetases (aaRSs) establish the genetic code. Each aaRS covalently links a given canonical amino acid to a cognate set of tRNA isoacceptors. Glycyl tRNA aminoacylation is unusual in that it is catalyzed by different aaRSs in different lineages of the Tree of Life. We have investigated the phylogenetic distribution and evolutionary history of bacterial glycyl tRNA synthetase (bacGlyRS). This enzyme is found in early diverging bacterial phyla such as Firmicutes, Acidobacteria, and Proteobacteria, but not in archaea or eukarya. We observe relationships between each of six domains of bacGlyRS and six domains of four different RNA‐modifying proteins. Component domains of bacGlyRS show common ancestry with i) the catalytic domain of class II tRNA synthetases; ii) the HD domain of the bacterial RNase Y; iii) the body and tail domains of the archaeal CCA‐adding enzyme; iv) the anti‐codon binding domain of the arginyl tRNA synthetase; and v) a previously unrecognized domain that we call ATL (Ancient tRNA latch). The ATL domain is found only in bacGlyRS and in the universal alanyl tRNA synthetase (uniAlaRS). Further, the catalytic domain of bacGlyRS is more closely related to the catalytic domain of uniAlaRS than to any other aminoacyl tRNA synthetase. The combined data suggest that the ATL and catalytic domains of these two enzymes are ancestral to bacGlyRS and uniAlaRS, which emerged from common protein ancestors by bricolage, stepwise accumulation of protein domains, before the last universal common ancestor of life.This article is protected by copyright. All rights reserved.

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A genomic database furnishes minimal functional glycyl-tRNA synthetases homologous to other, designed class II urzymes

Patra,

Douglas,

Wills

et al. 2024

Nucleic Acids Research

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The hypothesis that conserved core catalytic sites could represent ancestral aminoacyl-tRNA synthetases (AARS) drove the design of functional TrpRS, LeuRS, and HisRS ‘urzymes’. We describe here new urzymes detected in the genomic record of the arctic fox, Vulpes lagopus. They are homologous to the α-subunit of bacterial heterotetrameric Class II glycyl-tRNA synthetase (GlyRS-B) enzymes. AlphaFold2 predicted that the N-terminal 81 amino acids would adopt a 3D structure nearly identical to our designed HisRS urzyme (HisCA1). We expressed and purified that N-terminal segment and the spliced open reading frame GlyCA1–2. Both exhibit robust single-turnover burst sizes and ATP consumption rates higher than those previously published for HisCA urzymes and comparable to those for LeuAC and TrpAC. GlyCA is more than twice as active in glycine activation by adenosine triphosphate as the full-length GlyRS-B α2 dimer. Michaelis–Menten rate constants for all three substrates reveal significant coupling between Exon2 and both substrates. GlyCA activation favors Class II amino acids that complement those favored by HisCA and LeuAC. Structural features help explain these results. These minimalist GlyRS catalysts are thus homologous to previously described urzymes. Their properties reinforce the notion that urzymes may have the requisite catalytic activities to implement a reduced, ancestral genetic coding alphabet.

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Mechanism of tRNA recognition by heterotetrameric glycyl-tRNA synthetase from lactic acid bacteria

Cited by 3 publications

References 47 publications

Common evolutionary origins of the bacterial glycyl tRNA synthetase and alanyl tRNA synthetase

Common evolutionary origins of the bacterial glycyl tRNA synthetase and alanyl tRNA synthetase

Common evolutionary origins of the bacterial glycyl tRNA synthetase and alanyl tRNA synthetase

A genomic database furnishes minimal functional glycyl-tRNA synthetases homologous to other, designed class II urzymes

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