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

Abstract

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 PabTrmU54) 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.

The archaeal COG1901/DUF358 SPOUT-methyltransferase members, together with pseudouridine synthase Pus10, catalyze the formation of 1-methylpseudouridine at position 54 of tRNA

“…1A; Table 1). Likewise, when a tRNA transcript specific for Phe, Asp, or Ile, lacking modifications, was incubated with AdoMet and cell extracts from P. furiosus or P. abyssi, m 5 U was almost quantitatively formed at position 54 of the TC-loop (Constantinesco et al 1999;Urbonavicius et al 2008). Under the same experimental conditions, U54 in the tRNA Ile transcript was shown to be ''doubly'' modified into m 1 C when incubated with cell extracts from H. volcanii (Grosjean et al 1995).…”

“…Under the same experimental conditions, U54 in the tRNA Ile transcript was shown to be ''doubly'' modified into m 1 C when incubated with cell extracts from H. volcanii (Grosjean et al 1995). The enzyme responsible for the formation of m 5 U54 in P. abyssi was recently identified as PAB_0719 (aTrmU54) (Urbonavicius et al 2008;Auxilien et al 2011). This protein is a member of the COG2265 SAM-dependent, Rossmannlike RNA m 5 U methyltransferase family.…”

“…jannaschii TrmY can produce m 1 C54 in full-sized tRNAs as well as at the equivalent position in TC-stemloop substrates (17-mer TC-arm of tRNA). Likewise, the tRNA:m 5 U54 methyltransferases of E. coli (TrmA or RumT), of S. cerevisiae (Trm2p), and of P. abyssi (PAB_0719, aTrmU54) can produce m 5 U54 in similar full-sized or truncated RNAs (Gu et al 1996;Becker et al 1997;Urbonavicius et al 2008), suggesting a possibility of similar substrate recognition modes as described for E. coli TrmA (Alian et al 2008) and archaeal TrmU54 ). However, archaeal TrmY can methylate C54 in tRNA harboring G58 and G60 (Fig.…”

“…NRC1, a different strain from H. cutirubrum, but with a sequenced genome was used to identify the presence of gene pus10, trmY, and trmU54. Numbers correspond to the following references: (1) (Noon et al 2003); (2) (Gupta and Woese 1980), m 1 C is listed as xU in this reference; (3) (Edmonds et al 1991); (4) (Kilpatrick and Walker 1981); (5) ; (6) (Best 1978), m 1 C was misidentified as dihydrouridine in this reference, due to their similar mobilities in TLC; (7) (Gu et al 1984); (8) (Gupta 1984); (9) (Gupta 1986); (10) (Pang et al 1982); (11) (Gu et al 1983); (12) (Nicoghosian et al 1985); (13) (Urbonavicius et al 2008); (14) (Constantinesco et al 1999); (15) (Kowalak et al 1994). Kowalak et al 1994;Constantinesco et al 1999).…”

Archaeal Pus10 proteins can produce both pseudouridine 54 and 55 in tRNA

“…Recently, it has been shown that homologs of the bacterial rumA gene, which encodes the enzyme for m 5 U1939 in Escherichia coli 23 rRNA, are present in Archaea, but only in the members of Thermococcales and Nanoarchaea. Moreover, the product of this rumA-type gene has in vitro AdoMet-dependent tRNA m 5 U54 activity (Urbonavicius et al 2008). Therefore, it is possible that most of the P. furiosus tRNAs contain m 5 U54, while a select few have C54, as is the case for higher eukaryotes (Sprinzl and Vassilenko 2005).…”