Acquisition of a bacterial RumA-type tRNA(uracil-54, C5)-methyltransferase by Archaea through an ancient horizontal gene transfer.

Jaunius Urbonavicius (1) , Sylvie Auxilien (1) , Hélène Walbott (1) , Kalliopi Trachana (1) , Béatrice Golinelli-Pimpaneau (1) , Céline Brochier-Armanet (2) , Henri Grosjean (3, 1)

1 LEBS - Laboratoire d'Enzymologie et Biochimie Structurales
2 EGEE - Evolution, Genome, Environnement
3 IGM - Institut de génétique et microbiologie [Orsay]

The Pyrococcus abyssi genome displays two genes possibly coding for S-adenosyl-l-methionine-dependent RNA(uracil, C5)-methyltransferases (PAB0719 and PAB0760). Their amino acid sequences are more closely related to Escherichia coli RumA catalysing the formation of 5-methyluridine (m(5)U)-1939 in 23S rRNA than to E. coli TrmA (tRNA methyltransferase A) methylating uridine-54 in tRNA. Comparative genomic and phylogenetic analyses show that homologues of PAB0719 and PAB0760 occur only in a few Archaea, these genes having been acquired via a single horizontal gene transfer from a bacterial donor to the common ancestor of Thermococcales and Nanoarchaea. This transfer event was followed by a duplication event in Thermococcales leading to two closely related genes. None of the gene products of the two P. abyssi paralogues catalyses in vitro the formation of m(5)U in a P. abyssi rRNA fragment homologous to the bacterial RumA substrate. Instead, PAB0719 enzyme (renamed (Pab)TrmU54) displays an identical specificity to TrmA, as it catalyses the in vitro formation of m(5)U-54 in tRNA. Thus, during evolution, at least one of the two P. abyssi RumA-type enzymes has changed of target specificity. This functional shift probably occurred in an ancestor of all Thermococcales. This study also provides new evidence in favour of a close relationship between Thermococcales and Nanoarchaea.

Domaines: Biochimie, Biologie Moléculaire; Microbiologie et Parasitologie; Biochimie [q-bio.BM]; Biologie moléculaire; Sciences du Vivant [q-bio]

Jaunius Urbonavicius, Sylvie Auxilien, Hélène Walbott, Kalliopi Trachana, Béatrice Golinelli-Pimpaneau, et al.. Acquisition of a bacterial RumA-type tRNA(uracil-54, C5)-methyltransferase by Archaea through an ancient horizontal gene transfer.. Molecular Microbiology, 2008, 67 (2), pp.323-35. ⟨10.1111/j.1365-2958.2007.06047.x⟩. ⟨hal-02287548⟩