title: Trans-oligomerization of duplicated aminoacyl-tRNA synthetases maintains genetic code fidelity under stress.
abstract: Aminoacyl-tRNA synthetases (aaRSs) play a key role in deciphering the genetic message by producing charged tRNAs and are equipped with proofreading mechanisms to ensure correct pairing of tRNAs with their cognate amino acid. Duplicated aaRSs are very frequent in Nature, with 25,913 cases observed in 26,837 genomes. The oligomeric nature of many aaRSs raises the question of how the functioning and oligomerization of duplicated enzymes is organized. We characterized this issue in a model prokaryotic organism that expresses two different threonyl-tRNA synthetases, responsible for Thr-tRNA(Thr) synthesis: one accurate and constitutively expressed (T1) and another (T2) with impaired proofreading activity that also generates mischarged Ser-tRNA(Thr). Low zinc promotes dissociation of dimeric T1 into monomers deprived of aminoacylation activity and simultaneous induction of T2, which is active for aminoacylation under low zinc. T2 either forms homodimers or heterodimerizes with T1 subunits that provide essential proofreading activity in trans. These findings evidence that in organisms with duplicated genes, cells can orchestrate the assemblage of aaRSs oligomers that meet the necessities of the cell in each situation. We propose that controlled oligomerization of duplicated aaRSs is an adaptive mechanism that can potentially be expanded to the plethora of organisms with duplicated oligomeric aaRSs.
authors.affiliation: Instituto de Bioquímica Vegetal y Fotosíntesis, C.S.I.C. and Universidad de Sevilla, Avda Américo Vespucio 49, E-41092 Seville, Spain.
authors.forename: Miguel Ángel
authors.initials: MÁ
authors.lastname: Rubio
authors.affiliation: Instituto de Bioquímica Vegetal y Fotosíntesis, C.S.I.C. and Universidad de Sevilla, Avda Américo Vespucio 49, E-41092 Seville, Spain.
authors.forename: Mauro
authors.initials: M
authors.lastname: Napolitano
authors.affiliation: Facultad de Formación del Profesorado. Universidad de Extremadura, Avda de la Universidad s/n. E-10003, Cáceres, Spain.
authors.forename: Jesús A G
authors.initials: JA
authors.lastname: Ochoa de Alda
authors.affiliation: Instituto de Bioquímica Vegetal y Fotosíntesis, C.S.I.C. and Universidad de Sevilla, Avda Américo Vespucio 49, E-41092 Seville, Spain.
authors.forename: Javier
authors.initials: J
authors.lastname: Santamaría-Gómez
authors.affiliation: SBBS and Chemistry, Durham University, Durham DH1 BLE, UK.
authors.forename: Carl J
authors.initials: CJ
authors.lastname: Patterson
authors.affiliation: SBBS and Chemistry, Durham University, Durham DH1 BLE, UK.
authors.forename: Andrew W
authors.initials: AW
authors.lastname: Foster
authors.affiliation: Department of Agrochemistry and Biochemistry, Faculty of Science, University of Alicante, E-03080, Spain.
authors.forename: Roque
authors.initials: R
authors.lastname: Bru-Martínez
authors.affiliation: SBBS and Chemistry, Durham University, Durham DH1 BLE, UK.
authors.forename: Nigel J
authors.initials: NJ
authors.lastname: Robinson
authors.affiliation: Instituto de Bioquímica Vegetal y Fotosíntesis, C.S.I.C. and Universidad de Sevilla, Avda Américo Vespucio 49, E-41092 Seville, Spain ignacio.luque@ibvf.csic.es.
authors.forename: Ignacio
authors.initials: I
authors.lastname: Luque
mesh_terms: D000604:Amino Acyl-tRNA Synthetases / Q000235:genetics / Q000378:metabolism; D017033:Anabaena / Q000201:enzymology / Q000235:genetics; D020131:Genes, Duplicate; D005815:Genetic Code; D007527:Isoenzymes / Q000235:genetics / Q000378:metabolism; D055503:Protein Multimerization; D017393:RNA Editing; D013312:Stress, Physiological / Q000235:genetics; D013914:Threonine-tRNA Ligase / Q000235:genetics* / Q000378:metabolism*; D015032:Zinc / Q000378:metabolism
chemical_list: D007527:Isoenzymes; D000604:Amino Acyl-tRNA Synthetases; D013914:Threonine-tRNA Ligase; D015032:Zinc