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Title: Structural insights into the polyphyletic origins of glycyl tRNA synthetases

Glycyl tRNA synthetase (GlyRS) provides a unique case among class II aminoacyl tRNA synthetases, with two clearly widespread types of enzymes: a dimeric (α 2) species present in some bacteria, archaea, and eukaryotes; and a heterotetrameric form (α 2β 2) present in most bacteria. Although the differences between both types of GlyRS at the anticodon binding domain level are evident, the extent and implications of the variations in the catalytic domain have not been described, and it is unclear whether the mechanism of amino acid recognition is also dissimilar. Here, we show that the α-subunit of the α 2β 2 GlyRS from the bacterium Aquifex aeolicus is able to perform the first step of the aminoacylation reaction, which involves the activation of the amino acid with ATP. The crystal structure of the α-subunit in the complex with an analog of glycyl adenylate at 2.8 Å resolution presents a conformational arrangement that properly positions the cognate amino acid. This work shows that glycine is recognized by a subset of different residues in the two types of GlyRS. Furthermore, a structural and sequence analysis of class II catalytic domains shows that bacterial GlyRS is closely related to alanyl tRNA synthetase, which ledmore » us to define a new subclassification of these ancient enzymes and to propose an evolutionary path of α 2β 2 GlyRS, convergent with α 2 GlyRS and divergent from AlaRS, thus providing a possible explanation for the puzzling existence of two proteins sharing the same fold and function but not a common ancestor.« less
Authors:
 [1] ;  [2] ;  [3] ;  [1] ;  [1] ;  [4] ;  [5] ;  [5] ; ORCiD logo [6] ; ORCiD logo [6] ;  [7] ;  [3] ; ORCiD logo [1]
  1. Univ. Nacional Autonoma de Mexico, Mexico City (Mexico)
  2. Univ. Nacional Autonoma de Mexico, Mexico City (Mexico); Centro de Investigacion y Estudios Avanzados del Instituto Politecnico Nacional, Guanajuato (Mexico)
  3. Univ. of Gothenburg, Gothenburg (Sweden)
  4. Lab. de Biologie Integrative des Milieux Marins, Roscoff (France)
  5. Institute of Genetics and of Molecular and Cellular Biology, Illkirch (France)
  6. European Molecular Biology Lab., Hamburg (Germany)
  7. Centro de Investigacion y Estudios Avanzados del Instituto Politecnico Nacional, Guanajuato (Mexico)
Publication Date:
Grant/Contract Number:
AC02-06CH11357; 085P1000817
Type:
Accepted Manuscript
Journal Name:
Journal of Biological Chemistry
Additional Journal Information:
Journal Volume: 291; Journal Issue: 28; Journal ID: ISSN 0021-9258
Publisher:
American Society for Biochemistry and Molecular Biology
Research Org:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org:
USDOE Office of Science (SC)
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; aminoacyl tRNA synthetase; crystal structure; molecular evolution; structure-function; substrate specificity
OSTI Identifier:
1267479

Valencia-Sánchez, Marco Igor, Rodríguez-Hernández, Annia, Ferreira, Ruben, Santamaría-Suárez, Hugo Aníbal, Arciniega, Marcelino, Dock-Bregeon, Anne-Catherine, Moras, Dino, Beinsteiner, Brice, Mertens, Haydyn, Svergun, Dmitri, Brieba, Luis G., Grøtli, Morten, and Torres-Larios, Alfredo. Structural insights into the polyphyletic origins of glycyl tRNA synthetases. United States: N. p., Web. doi:10.1074/jbc.M116.730382.
Valencia-Sánchez, Marco Igor, Rodríguez-Hernández, Annia, Ferreira, Ruben, Santamaría-Suárez, Hugo Aníbal, Arciniega, Marcelino, Dock-Bregeon, Anne-Catherine, Moras, Dino, Beinsteiner, Brice, Mertens, Haydyn, Svergun, Dmitri, Brieba, Luis G., Grøtli, Morten, & Torres-Larios, Alfredo. Structural insights into the polyphyletic origins of glycyl tRNA synthetases. United States. doi:10.1074/jbc.M116.730382.
Valencia-Sánchez, Marco Igor, Rodríguez-Hernández, Annia, Ferreira, Ruben, Santamaría-Suárez, Hugo Aníbal, Arciniega, Marcelino, Dock-Bregeon, Anne-Catherine, Moras, Dino, Beinsteiner, Brice, Mertens, Haydyn, Svergun, Dmitri, Brieba, Luis G., Grøtli, Morten, and Torres-Larios, Alfredo. 2016. "Structural insights into the polyphyletic origins of glycyl tRNA synthetases". United States. doi:10.1074/jbc.M116.730382. https://www.osti.gov/servlets/purl/1267479.
@article{osti_1267479,
title = {Structural insights into the polyphyletic origins of glycyl tRNA synthetases},
author = {Valencia-Sánchez, Marco Igor and Rodríguez-Hernández, Annia and Ferreira, Ruben and Santamaría-Suárez, Hugo Aníbal and Arciniega, Marcelino and Dock-Bregeon, Anne-Catherine and Moras, Dino and Beinsteiner, Brice and Mertens, Haydyn and Svergun, Dmitri and Brieba, Luis G. and Grøtli, Morten and Torres-Larios, Alfredo},
abstractNote = {Glycyl tRNA synthetase (GlyRS) provides a unique case among class II aminoacyl tRNA synthetases, with two clearly widespread types of enzymes: a dimeric (α2) species present in some bacteria, archaea, and eukaryotes; and a heterotetrameric form (α2β2) present in most bacteria. Although the differences between both types of GlyRS at the anticodon binding domain level are evident, the extent and implications of the variations in the catalytic domain have not been described, and it is unclear whether the mechanism of amino acid recognition is also dissimilar. Here, we show that the α-subunit of the α2β2 GlyRS from the bacterium Aquifex aeolicus is able to perform the first step of the aminoacylation reaction, which involves the activation of the amino acid with ATP. The crystal structure of the α-subunit in the complex with an analog of glycyl adenylate at 2.8 Å resolution presents a conformational arrangement that properly positions the cognate amino acid. This work shows that glycine is recognized by a subset of different residues in the two types of GlyRS. Furthermore, a structural and sequence analysis of class II catalytic domains shows that bacterial GlyRS is closely related to alanyl tRNA synthetase, which led us to define a new subclassification of these ancient enzymes and to propose an evolutionary path of α2β2 GlyRS, convergent with α2 GlyRS and divergent from AlaRS, thus providing a possible explanation for the puzzling existence of two proteins sharing the same fold and function but not a common ancestor.},
doi = {10.1074/jbc.M116.730382},
journal = {Journal of Biological Chemistry},
number = 28,
volume = 291,
place = {United States},
year = {2016},
month = {5}
}

Works referenced in this record:

DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering
journal, January 2009
  • Franke, Daniel; Svergun, Dmitri I.
  • Journal of Applied Crystallography, Vol. 42, Issue 2, p. 342-346
  • DOI: 10.1107/S0021889809000338

Determination of the regularization parameter in indirect-transform methods using perceptual criteria
journal, August 1992

PRIMUS: a Windows PC-based system for small-angle scattering data analysis
journal, September 2003
  • Konarev, Petr V.; Volkov, Vladimir V.; Sokolova, Anna V.
  • Journal of Applied Crystallography, Vol. 36, Issue 5, p. 1277-1282
  • DOI: 10.1107/S0021889803012779

A small and robust active beamstop for scattering experiments on high-brilliance undulator beamlines
journal, February 2015
  • Blanchet, Clement E.; Hermes, Christoph; Svergun, Dmitri I.
  • Journal of Synchrotron Radiation, Vol. 22, Issue 2, p. 461-464
  • DOI: 10.1107/S160057751402829X

Coot model-building tools for molecular graphics
journal, November 2004
  • Emsley, Paul; Cowtan, Kevin
  • Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
  • DOI: 10.1107/S0907444904019158

PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
  • Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
  • DOI: 10.1107/S0907444909052925

Automated matching of high- and low-resolution structural models
journal, February 2001

Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs
journal, September 1990
  • Eriani, Gilbert; Delarue, Marc; Poch, Olivier
  • Nature, Vol. 347, Issue 6289, p. 203-206
  • DOI: 10.1038/347203a0