Biosynthesis of Archaeosine, a Novel Derivative of 7-Deazaguanosine Specific to Archaeal tRNA, Proceeds via a Pathway Involving Base Replacement on the tRNA Polynucleotide Chain

Watanabe, Masakatsu; Matsuo, Mami; Tanaka, Sonoko; Akimoto, Hiroshi; Asahi, Shuichi; Nishimura, Susumu; Katze, Jon R.; Hashizume, Takeshi; Crain, Pamela F.; McCloskey, James A.; Okada, Norihiro

doi:10.1074/jbc.272.32.20146

Cited by 78 publications

(84 citation statements)

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“…Because preQ 0 is known to be an intermediate in the formation of the ubiquitous archaeal tRNA-modified nucleoside archaeosine (18), Q and archaeosine may share a common 7-deazaguanosine biosynthesis pathway. Examination of the genomes of archae indicates that these organisms contain the ykvJ, K, and L homologs but are missing the ykvM homolog (except in Aeropyrum pernix) that is believed to be a GTP cyclohydrolase homolog (see above).…”

Section: Discussionmentioning

confidence: 99%

“…A second 7-deazaguanosine tRNA modification, archaeosine, is found in all archaeal tRNAs at position 15 of the D-loop (17). Archaeosine is also synthesized via preQ 0 , the substrate for the archaea, TGT enzyme (18). Although the TGT-dependent guanine exchange reactions are well characterized for both Q and archaeosine biosynthesis, little is known about the enzymes and intermediates involved in carbon atom replacement of N-7 of the purine ring to produce 7-deazaguanosine bases preQ 0 and preQ 1 .…”

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confidence: 99%

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Identification of Four Genes Necessary for Biosynthesis of the Modified Nucleoside Queuosine

Reader

Metzgar

Schimmel

et al. 2004

Journal of Biological Chemistry

138

134

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Queuosine (Q) is a hypermodified 7-deazaguanosine nucleoside located in the anticodon wobble position of four amino acid-specific tRNAs. In bacteria, Q is produced de novo from GTP via the 7-deazaguanosine precursor preQ 1 (7-aminoethyl 7-deazaguanine) by an uncharacterized pathway. PreQ 1 is subsequently transferred to its specific tRNA by a tRNA-guanine transglycosylase (TGT) and then further modified in situ to produce Q. Here we use comparative genomics to implicate four gene families (best exemplified by the B. subtilis operon ykvJKLM) as candidates in the preQ 1 biosynthetic pathway. Deletions were constructed in genes for each of the four orthologs in Acinetobacter. High pressure liquid chromatography analysis showed the Q nucleoside was absent from the tRNAs of each of four deletion strains. Electrospray ionization mass spectrometry confirmed the absence of Q in each mutant strain. Finally, introduction of the Bacillus subtilis ykvJKLM operon in trans complemented the Q deficiency of the two deletion mutants that were tested. Thus, the products of these four genes (named queC, -D, -E, and -F) are essential for the Q biosynthetic pathway.Nucleoside modification typically occurs in ϳ10% of the nucleosides of a particular tRNA but can involve as many as 25% of the nucleosides for a specific tRNA (1). Over 80 modified nucleosides have been characterized (1), many of which are phylogenetically conserved. The nature of nucleoside modification varies from simple methylation of the base or ribose ring to extensive "hypermodification" of the canonical bases. The latter involves multiple enzymatic steps and can result in substantive structural changes (2). Queuosine (Q) 1 is an example of a highly modified nucleoside located in the anticodon wobble position 34 of tRNAs specific for Tyr, His, Asp, and Asn (3). With few exceptions (such as yeast and mycoplasma), it is widely distributed in most prokaryotic and eukaryotic phyla (4). Q is based on a very unusual 7-deazaguanosine core, which is further modified by addition of a cyclopentendiol ring (5, 6). The Q modification has long been known and has been implicated in a number of disparate physiological phenomena, such as eukaryotic cell proliferation and differentiation (7-10), tyrosine biosynthesis (11), and bacterial virulence (12). However, despite the presence of Q in the tRNA anticodon loop, no definitive role for Q in translation has been established (13).Unlike eukaryotes that import the queuine base, bacteria synthesize Q modification de novo from a GTP starting block (14). The first stage of synthesis gives 7-cyano-7-deazaguanosine (preQ 0 ) that is then further modified into 7-aminoethyl 7-deazaguanine (preQ 1 ) (Fig. 1). The preQ 1 base is subsequently transferred to the appropriate tRNA in a guanine-exchange reaction catalyzed by a tRNA-guanine transglycosylase (TGT) (15). It is then further modified in situ to give Q (16). A second 7-deazaguanosine tRNA modification, archaeosine, is found in all archaeal tRNAs at position 15 of the D-loop (17). Archa...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Identification of Four Genes Necessary for Biosynthesis of the Modified Nucleoside Queuosine

Reader

Metzgar

Schimmel

et al. 2004

Journal of Biological Chemistry

138

134

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“…9). In Archaea, the tRNA guanosine (15) transglycosylase enzyme (aTGT; EC 2.4.2.48) is homologous to the bTGT enzyme and exchanges the G at position 15 with preQ 0 in nearly all tRNAs (15,16). The preQ 0 is then modified to G + by different types of amidotransferases [archaeosine synthase (ArcS), QueF-like, and glutamine amidotransferase class-II (GAT)-QueC] (17,18) (Fig.…”

Section: Significancementioning

confidence: 99%

Novel genomic island modifies DNA with 7-deazaguanine derivatives

Thiaville

Kellner

Yuan

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

161

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The discovery of ∼20-kb gene clusters containing a family of paralogs of tRNA guanosine transglycosylase genes, called tgtA5, alongside 7-cyano-7-deazaguanine (preQ 0 ) synthesis and DNA metabolism genes, led to the hypothesis that 7-deazaguanine derivatives are inserted in DNA. This was established by detecting 2'-deoxy-preQ 0 and 2'-deoxy-7-amido-7-deazaguanosine in enzymatic hydrolysates of DNA extracted from the pathogenic, Gram-negative bacteria Salmonella enterica serovar Montevideo. These modifications were absent in the closely related S. enterica serovar Typhimurium LT2 and from a mutant of S. Montevideo, each lacking the gene cluster. This led us to rename the genes of the S. Montevideo cluster as dpdA-K for 7-deazapurine in DNA. Similar gene clusters were analyzed in ∼150 phylogenetically diverse bacteria, and the modifications were detected in DNA from other organisms containing these clusters, including Kineococcus radiotolerans, Comamonas testosteroni, and Sphingopyxis alaskensis. Comparative genomic analysis shows that, in Enterobacteriaceae, the cluster is a genomic island integrated at the leuX locus, and the phylogenetic analysis of the TgtA5 family is consistent with widespread horizontal gene transfer. Comparison of transformation efficiencies of modified or unmodified plasmids into isogenic S. Montevideo strains containing or lacking the cluster strongly suggests a restriction-modification role for the cluster in Enterobacteriaceae. Another preQ 0 derivative, 2'-deoxy-7-formamidino-7-deazaguanosine, was found in the Escherichia coli bacteriophage 9g, as predicted from the presence of homologs of genes involved in the synthesis of the archaeosine tRNA modification. These results illustrate a deep and unexpected evolutionary connection between DNA and tRNA metabolism.DNA modification | restriction-modification | 7-deazaguanine | comparative genomics | queuosine H ypermodifications of DNA requiring more than one synthetic enzyme are not as prevalent and chemically diverse as RNA hypermodifications, but around a dozen have been identified in DNA to date (1). The functions of most DNA hypermodifications are still not known, but some have roles in protection against restriction enzymes, whereas others affect thermal stability temperature, DNA packaging, or transcription regulation (2). For example, the hypermodified DNA base β-D-glucosyl-hydroxymethyluracil, or base J, is an epigenetic factor that regulates Pol II transcription initiation in kinetoplastids of trypanosomes (3). The recently discovered phosphorothioate (PT) modification of the DNA backbone in bacteria was found to perform different functions in different organisms (4-6). In Salmonella Cerro 87, PT occurs on each strand of a GAAC/GTTC motif as part of a restriction-modification (R-M) system, whereas in Vibrio cyclitrophicus FF75, which lacks PT restriction enzymes, PT occurs on one strand of C ps CA motifs, and the function remains unclear (6). In 2013, Iyer et al. described the computational prediction of 12 novel DNA hypermodificat...

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“…In this proposal, the steps leading to preQ 0 are presumably identical in both the archaea and bacteria (eukarya are incapable of de novo biosynthesis of queuosine (8)) and diverge at preQ 0 , with preQ 0 (or a related metabolite such as the amide or archaeosine base) serving as the substrate for an archaeal TGT in the key base substitution reaction. This proposal was strengthened with the identification of an open reading frame (MJ0436) with high sequence homology to the Escherichia coli TGT in the genome of the archaeal hyperthermophile Methanococcus jannaschii (19) and the subsequent isolation of an archaeal TGT enzyme from Haloferax valcanii (20).…”

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confidence: 99%

Hypermodification of tRNA in Thermophilic Archaea

Bai

Fox

Lacy

et al. 2000

Journal of Biological Chemistry

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tRNA is structurally unique among nucleic acids in harboring an astonishing diversity of modified nucleosides. Two structural variants of the hypermodified nucleoside 7-deazaguanosine have been identified in tRNA: queuosine, which is found at the wobble position of the anticodon in bacterial and eukaryotic tRNA, and archaeosine, which is found at position 15 of the D-loop in archaeal tRNA. From homology searching of the Methanococcus jannaschii genome, a gene coding for an enzyme in the biosynthesis of archaeosine (tgt) was identified and cloned. The tgt gene was overexpressed in an Escherichia coli expression system, and the recombinant tRNA-guanine transglycosylase enzyme was purified and characterized. The enzyme catalyzes a transglycosylation reaction in which guanine is eliminated from position 15 of the tRNA and an archaeosine precursor (preQ 0 ) is inserted. The enzyme is able to utilize both guanine and the 7-deazaguanine base preQ 0 as substrates, but not other 7-deazaguanine bases, and is able to modify tRNA from all three phylogenetic domains. The enzyme shows optimal activity at high temperature and acidic pH, consistent with the optimal growth conditions of M. jannaschii. The nature of the temperature dependence is consistent with a requirement for some degree of tRNA tertiary structure in order for recognition by the enzyme to occur.

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Biosynthesis of Archaeosine, a Novel Derivative of 7-Deazaguanosine Specific to Archaeal tRNA, Proceeds via a Pathway Involving Base Replacement on the tRNA Polynucleotide Chain

Cited by 78 publications

References 56 publications

Identification of Four Genes Necessary for Biosynthesis of the Modified Nucleoside Queuosine

Identification of Four Genes Necessary for Biosynthesis of the Modified Nucleoside Queuosine

Novel genomic island modifies DNA with 7-deazaguanine derivatives

Hypermodification of tRNA in Thermophilic Archaea

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