Acquisition of a bacterial RumA-type tRNA(uracil-54, C5)-methyltransferase by Archaea through an ancient horizontal gene transfer.
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.
Urbonavicius
Jaunius
J
Laboratoire d'Enzymologie et Biochimie Structurales, CNRS, 1 avenue de la Terrasse, 91190, Gif-sur-Yvette, France.
Auxilien
Sylvie
S
Walbott
Hélène
H
Trachana
Kalliopi
K
Golinelli-Pimpaneau
Béatrice
B
Brochier-Armanet
Céline
C
Grosjean
Henri
H
D001105:Archaea / Q000145:classification / Q000201:enzymology* / Q000235:genetics*; D001419:Bacteria / Q000235:genetics; D001426:Bacterial Proteins / Q000235:genetics*; D001483:Base Sequence; D019295:Computational Biology; D017124:Conserved Sequence; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal; D020745:Genome, Archaeal; D007501:Iron / Q000378:metabolism; D008274:Magnesium / Q000378:metabolism; D008745:Methylation; D008969:Molecular Sequence Data; D046588:Nanoarchaeota / Q000235:genetics; D010802:Phylogeny; D043903:Pyrococcus abyssi / Q000235:genetics; D012343:RNA, Transfer / Q000378:metabolism; D011993:Recombinant Fusion Proteins / Q000302:isolation & purification / Q000378:metabolism; D013455:Sulfur / Q000378:metabolism; D019709:Thermococcales / Q000235:genetics; D014498:Uracil / Q000378:metabolism; D014529:Uridine / Q000378:metabolism; D012359:tRNA Methyltransferases / Q000235:genetics* / Q000378:metabolism
D001426:Bacterial Proteins; D011993:Recombinant Fusion Proteins; C093591:RumA protein, Bacteria; D014498:Uracil; D013455:Sulfur; D012343:RNA, Transfer; D007501:Iron; D012359:tRNA Methyltransferases; D008274:Magnesium; D014529:Uridine