Structural insights into the polyphyletic origins of glycyl tRNA synthetases

Valencia-Sánchez, Marco Igor; Rodríguez-Hernández, Annia; Ferreira, Ruben; Santamaría-Suárez, Hugo AnÃ­bal; Arciniega, Marcelino; Dock-Bregeon, Anne-Catherine; Moras, Dino; Beinsteiner, Brice; Mertens, Haydyn; Svergun, Dmitri; Brieba, Luis G.; Grøtli, Morten; Torres-Larios, Alfredo

doi:10.1074/jbc.M116.730382

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

Journal Article · Mon May 23 00:00:00 EDT 2016 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.M116.730382· OSTI ID:1267479

Valencia-Sánchez, Marco Igor ^[1]; Rodríguez-Hernández, Annia ^[2]; Ferreira, Ruben ^[3]; Santamaría-Suárez, Hugo AnÃbal ^[1]; Arciniega, Marcelino ^[1]; Dock-Bregeon, Anne-Catherine ^[4]; Moras, Dino ^[5]; Beinsteiner, Brice ^[5];

^[6];

^[6]; Brieba, Luis G. ^[7]; Grøtli, Morten ^[3];

^[1]

Univ. Nacional Autonoma de Mexico, Mexico City (Mexico)
Univ. Nacional Autonoma de Mexico, Mexico City (Mexico); Centro de Investigacion y Estudios Avanzados del Instituto Politecnico Nacional, Guanajuato (Mexico)
Univ. of Gothenburg, Gothenburg (Sweden)
Lab. de Biologie Integrative des Milieux Marins, Roscoff (France)
Institute of Genetics and of Molecular and Cellular Biology, Illkirch (France)
European Molecular Biology Lab., Hamburg (Germany)
Centro de Investigacion y Estudios Avanzados del Instituto Politecnico Nacional, Guanajuato (Mexico)

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.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-06CH11357; 085P1000817

OSTI ID:: 1267479

Journal Information:: Journal of Biological Chemistry, Vol. 291, Issue 28; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 10 works

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59 BASIC BIOLOGICAL SCIENCES
60 APPLIED LIFE SCIENCES
aminoacyl tRNA synthetase
crystal structure
molecular evolution
structure-function
substrate specificity