Biosynthesis of 4-Thiouridine in tRNA in the Methanogenic Archaeon Methanococcus maripaludis

Liu, Yuchen; Zhu, Xiang; Nakamura, Akiyoshi; Orlando, Ron; Söll, Dieter; Whitman, William B.

doi:10.1074/jbc.m112.405688

Cited by 51 publications

(62 citation statements)

References 64 publications

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“…A single mutation of any of the three Cys removed protein-bound Fe, suggesting that these Cys residues chelate the Fe-S cluster. A trisulfide linkage was previously detected in the CXXC motif by mass spectrometry analyses of M. maripaludis ThiI, M. maripaludis Ncs6 homolog, and M. jannaschii SepCysS (30,32,36); however, the sulfane sulfur (S 0 ) carried by Cys may come from oxidation of an Fe-S cluster, which was similarly observed upon oxidative decomposition of a spinach ferredoxin (42) and aconitase (43). The three conserved Cys residues are essential for in vivo activities of M. maripaludis ThiI (32) and M. jannaschii SepCysS (36).…”

Section: Discussionmentioning

confidence: 99%

“…1B). A single mutation of any of the three Cys abolished M. maripaludis ThiI activity (32), demonstrating that all three Cys residues are crucial. This three-conserved Cys pattern is also present in SeptRNA:Cys-tRNA synthase (SepCysS), which catalyzes tRNAdependent Cys biosynthesis in methanogenic archaea ( Fig.…”

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confidence: 97%

“…The importance of the Fe-S cluster for M. maripaludis ThiI enzyme activity was examined using [(N-acryloylamino)phenyl] mercuric chloride (APM) gel electrophoresis, a method that detects sulfur modifications in RNAs (40). Cysteine, thiosulfate, thiophosphate, and sulfide were previously tested as possible sulfur sources, but only sulfide supported the formation of thiolated tRNA exhibiting retarded migration in APM gels (32). The K M of Na 2 S (∼1 mM) (32) is close to the estimated intracellular concentrations of free sulfide in methanococci (∼1-3 mM) (41), suggesting that sulfide is a physiologically relevant sulfur donor.…”

Section: Thii Sepcyss and The Ncs6 Homolog In Methanogenic Archaeamentioning

confidence: 99%

“…This is based on the observations that: (i) the ncs6 gene homologs are widespread in archaeal genomes (23) (32). However, the E. coli s 4 U biosynthesis mechanism cannot fully explain the archaeal process because the gene encoding a cysteine desulfurase is missing in many sequenced archaeal genomes (23,33) and most archaeal ThiI homologs lack the RHD essential to transfer sulfur.…”

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confidence: 99%

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A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes

Liu

Vinyard

Reesbeck

et al. 2016

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

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The sulfur-containing nucleosides in transfer RNA (tRNAs) are present in all three domains of life; they have critical functions for accurate and efficient translation, such as tRNA structure stabilization and proper codon recognition. The tRNA modification enzymes ThiI (in bacteria and archaea) and Ncs6 (in archaea and eukaryotic cytosols) catalyze the formation of 4-thiouridine (s 4 U) and 2-thiouridine (s 2 U), respectively. The ThiI homologs were proposed to transfer sulfur via cysteine persulfide enzyme adducts, whereas the reaction mechanism of Ncs6 remains unknown. Here we show that ThiI from the archaeon Methanococcus maripaludis contains a [3Fe-4S] cluster that is essential for its tRNA thiolation activity. Furthermore, the archaeal and eukaryotic Ncs6 homologs as well as phosphoseryl-tRNA (Sep-tRNA):Cys-tRNA synthase (SepCysS), which catalyzes the Sep-tRNA to Cys-tRNA conversion in methanogens, also possess a [3Fe-4S] cluster similar to the methanogenic archaeal ThiI. These results suggest that the diverse tRNA thiolation processes in archaea and eukaryotic cytosols share a common mechanism dependent on a [3Fe-4S] cluster for sulfur transfer.iron-sulfur cluster | thionucleosides | tRNA modification | CTU1

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Section: Discussionmentioning

confidence: 99%

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confidence: 97%

Section: Thii Sepcyss and The Ncs6 Homolog In Methanogenic Archaeamentioning

confidence: 99%

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confidence: 99%

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A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes

Liu

Vinyard

Reesbeck

et al. 2016

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

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“…It is tempting to suggest that it is also the sulfur source in vivo. Free sulfide has been shown to be present at relatively high concentrations within thermophilic archaea (13) and participate in [Fe-S] cluster assembly as well as biosynthesis of methionine (14), thiamin thiazole (15), and U8-tRNA thiolation (16).…”

Section: Discussionmentioning

confidence: 99%

Nonredox thiolation in tRNA occurring via sulfur activation by a [4Fe-4S] cluster

Arragain

Bimaï

Legrand

et al. 2017

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

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Sulfur is present in several nucleosides within tRNAs. In particular, thiolation of the universally conserved methyl-uridine at position 54 stabilizes tRNAs from thermophilic bacteria and hyperthermophilic archaea and is required for growth at high temperature. The simple nonredox substitution of the C2-uridine carbonyl oxygen by sulfur is catalyzed by tRNA thiouridine synthetases called TtuA. Spectroscopic, enzymatic, and structural studies indicate that TtuA carries a catalytically essential [4Fe-4S] cluster and requires ATP for activity. A series of crystal structures shows that (i) the cluster is ligated by only three cysteines that are fully conserved, allowing the fourth unique iron to bind a small ligand, such as exogenous sulfide, and (ii) the ATP binding site, localized thanks to a proteinbound AMP molecule, a reaction product, is adjacent to the cluster. A mechanism for tRNA sulfuration is suggested, in which the unique iron of the catalytic cluster serves to bind exogenous sulfide, thus acting as a sulfur carrier.T he cellular translation machinery contains essential components such as tRNAs. To achieve their function, they feature a great variety of well-conserved posttranscriptional chemical modifications. Sulfur is present in several of these modified nucleosides: thiouridine and derivatives (s 4 U8, s 2 U34, and m 5 s 2 U54), 2-thioadenosine derivatives (ms 2 i 6 A37 and ms 2 t 6 A37), and 2-thiocytidine (s 2 C32). However, mechanisms of sulfur insertion into tRNAs are largely unknown, and the enzymes responsible for these reactions are incompletely characterized. Whereas redox conversion of a C-H to a C-S bond (synthesis of ms 2 i 6 A37 and ms 2 t 6 A37) depends on redox enzymes from the Radical-S-adenosyl-L-methionine iron-sulfur enzyme family, simple nonredox conversion of C = O to C = S group (synthesis of s 2 U34 and s 4 U8) is not expected to require such redox clusters. Intriguingly, we recently discovered that the ATPdependent formation of s 2 C32 in some tRNAs is catalyzed by an iron-sulfur enzyme, TtcA (1). However, the role of its cluster has not been defined. In the same superfamily, TtuA enzymes catalyze the C2-thiolation of uridine 54 in the T loop of thermophilic tRNAs (Fig. 1A), allowing stabilization of tRNAs at high temperature in thermophilic microorganisms. Sequences analysis shows that they share conserved cysteines and ATP binding motif (Fig. S1). Here, we report a detailed biochemical and structural characterization of TtuA that shows the presence of a [4Fe-4S] cluster essential for activity. The crystal structures of Pyrococcus horikoshii TtuA (PhTtuA) show that the cluster, chelated by only three cysteines, is adjacent to the ATP binding site. The presence of electron density near the fourth iron, nonbonded to the protein, indicates that the cluster can bind an exogenous substrate. We propose that thiolation occurs via sulfur binding to the cluster and transfer to the tRNA substrate. The fact that the catalytic [4Fe-4S] cluster serves as a sulfur carrier during a nonredox ...

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F430 Biosynthesis and Insertion

Mansoorabadi

Zheng

Ngo

2017

Encyclopedia of Inorganic and Bioinorganic Chemistry

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Methyl‐coenzyme M reductase (MCR) is the key enzyme of methanogenesis and the anaerobic oxidation of methane (AOM). MCR catalyzes the reversible conversion of methyl‐coenzyme M (MeS‐CoM) and coenzyme B (CoB‐SH) to the mixed heterodisulfide, CoB‐S‐S‐CoM, and methane. The methane forming and oxidizing activities of MCR are dependent on the unique, nickel‐containing tetrapyrrole, coenzyme F430. In addition to housing F430, the active site regions of MCR from both methanogens and anaerobic methanotrophic archaea (ANME) contain several unusual posttranslational modifications (PTMs). Given the unique ability of MCR to catalyze the AOM, there is much interest in the mechanism and formation of holo MCR for potential applications in gas‐to‐liquid (GTL) conversion strategies (see Methane‐to‐Methanol Conversion ). This chapter details current progress in the understanding of coenzyme F430 biosynthesis, the maturation of MCR, and differences in structural features of methanogenic and methanotrophic MCR that may be important for the AOM.

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Biosynthesis of 4-Thiouridine in tRNA in the Methanogenic Archaeon Methanococcus maripaludis

Cited by 51 publications

References 64 publications

A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes

A [3Fe-4S] cluster is required for tRNA thiolation in archaea and eukaryotes

Nonredox thiolation in tRNA occurring via sulfur activation by a [4Fe-4S] cluster

F430 Biosynthesis and Insertion

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