Biosynthesis of 4-thiouridine in tRNA in the methanogenic archaeon methanococcus maripaludis

Journal of Biological Chemistry

Volumn 287, Issue 44, 2012, Pages 36683-36692

  Liu, Yuchen ^a,b   Zhu, Xiang ^a   Nakamura, Akiyoshi ^b   Orlando, Ron ^a   Söll, Dieter ^b   Whitman, William B ^a  

^a UNIVERSITY OF GEORGIA   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEON; METHANOCOCCUS MARIPALUDIS; METHANOGENIC ARCHAEA; RELAY STRATEGIES; SULFUR TRANSFER;

BACTERIA; BIOCHEMISTRY; BIOSYNTHESIS; METABOLISM; METHANOGENS; PHYSIOLOGY;

SULFUR;

4 THIOURIDINE; CARBOXY TERMINAL TELOPEPTIDE; CYSTEINE; DISULFIDE; INORGANIC PYROPHOSPHATASE; SULFURTRANSFERASE; THIOSULFATE SULFURTRANSFERASE; THIOURIDINE; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SYNTHESIS; ESCHERICHIA COLI; GENE DELETION; IN VITRO STUDY; METHANOCOCCUS MARIPALUDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CARBON-SULFUR LYASES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ESCHERICHIA COLI; GENETIC COMPLEMENTATION TEST; METHANOCOCCUS; MODELS, BIOLOGICAL; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, TERTIARY; RNA, ARCHAEAL; RNA, TRANSFER; SULFIDES; SULFURTRANSFERASES; THIOURIDINE;

ARCHAEA; BACTERIA (MICROORGANISMS); METHANOCOCCUS MARIPALUDIS;

EID: 84868233239     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.405688     Document Type: Article

References (65)

1. Björk, G. R. (1995) Genetic dissection of synthesis and function of modified nucleosides in bacterial transfer RNA. Prog. Nucleic Acids Res. Mol. Biol. 50, 263-338
2. Thomas, G., and Favre, A. (1980) 4-Thiouridine triggers both growth delay induced by near-ultraviolet light and photoprotection. Eur. J. Biochem. 113, 67-74
3. Emilsson, V., Näslund, A. K., and Kurland, C. G. (1992) Thiolation of transferRNAin Escherichia coli varies with growth rate. Nucleic Acids Res. 20, 4499-4505
4. Kramer, G. F., Baker, J. C., and Ames, B. N. (1988) Near-UV stress in Salmonella typhimurium. 4-Thiouridine in tRNA, ppGpp, and ApppGpp as components of an adaptive response. J. Bacteriol. 170, 2344-2351
5. Favre, A., Yaniv, M., and Michelson, A. M. (1969) The photochemistry of 4-thiouridine in Escherichia coli t-RNAVal1. Biochem. Biophys. Res. Commun. 37, 266-271
6. Favre, A., Michelson, A. M., and Yaniv, M. (1971) Photochemistry of 4-thiouridine in Escherichia coli transfer RNA1Val. J. Mol. Biol. 58, 367-379
7. Thomas, G., and Favre, A. (1975) 4-Thiouridine as the target for nearultraviolet light-induced growth delay in Escherichia coli. Biochem. Biophys. Res. Commun. 66, 1454-1461
8. Carré, D. S., Thomas, G., and Favre, A. (1974) Conformation and functioning of tRNAs. Cross-linked tRNAs as substrate for tRNA nucleotidyl-transferase and aminoacyl synthetases. Biochimie 56, 1089-1101
9. Favre, A., Hajnsdorf, E., Thiam, K., and Caldeira de Araujo, A. (1985) Mutagenesis and growth delay induced in Escherichia coli by near-ultraviolet radiations. Biochimie 67, 335-342
10. Ramabhadran, T. V., and Jagger, J. (1976) Mechanism of growth delay induced in Escherichia coli by near ultraviolet radiation. Proc. Natl. Acad. Sci. U.S.A. 73, 59-63
11. Abrell, J. W., Kaufman, E. E., and Lipsett, M. N. (1971) The biosynthesis of 4-thiouridylate. J. Biol. Chem. 246, 294-301
12. Lipsett, M. N. (1978) Enzymes producing 4-thiouridine in Escherichia coli tRNA. Approximate chromosomal locations of the genes and enzyme activities in a 4-thiouridine-deficient mutant. J. Bacteriol. 135, 993-997
13. Kambampati, R., and Lauhon, C. T. (1999) IscS is a sulfurtransferase for the in vitro biosynthesis of 4-thiouridine in Escherichia coli tRNA. Biochemistry 38, 16561-16568
14. Lauhon, C. T., and Kambampati, R. (2000) The iscS gene in Escherichia coli is required for the biosynthesis of 4-thiouridine, thiamin, and NAD. J. Biol. Chem. 275, 20096-20103
15. Mueller, E. G., Buck, C. J., Palenchar, P. M., Barnhart, L. E., and Paulson, J. L. (1998) Identification of a gene involved in the generation of 4-thiouridine in tRNA. Nucleic Acids Res. 26, 2606-2610
16. Mueller, E. G. (2006) Trafficking in persulfides. Delivering sulfur in biosynthetic pathways. Nat. Chem. Biol. 2, 185-194
17. Zheng, L., White, R. H., Cash, V. L., and Dean, D. R. (1994) Mechanism for the desulfurization of L-cysteine catalyzed by the nifS gene product. Biochemistry 33, 4714-4720
18. Kessler, D. (2006) Enzymatic activation of sulfur for incorporation into biomolecules in prokaryotes. FEMS Microbiol. Rev. 30, 825-840
19. Schwartz, C. J., Djaman, O., Imlay, J. A., and Kiley, P. J. (2000) The cysteine desulfurase, IscS, has a major role in in vivo Fe-S cluster formation in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 97, 9009-9014
20. Lauhon, C. T. (2002) Requirement for IscS in biosynthesis of all thionucleosides in Escherichia coli. J. Bacteriol. 184, 6820-6829
21. Mihara, H., Kato, S., Lacourciere, G. M., Stadtman, T. C., Kennedy, R. A., Kurihara, T., Tokumoto, U., Takahashi, Y., and Esaki, N. (2002) The iscS gene is essential for the biosynthesis of 2-selenouridine in tRNA and the selenocysteine-containing formate dehydrogenase H. Proc. Natl. Acad. Sci. U.S.A. 99, 6679-6683
22. Zhang, W., Urban, A., Mihara, H., Leimkühler, S., Kurihara, T., and Esaki, N. (2010) IscS functions as a primary sulfur-donating enzyme by interacting specifically with MoeB and MoaD in the biosynthesis of molybdopterin in Escherichia coli. J. Biol. Chem. 285, 2302-2308
23. Nilsson, K., Lundgren, H. K., Hagervall, T. G., and Björk, G. R. (2002) The cysteine desulfurase IscS is required for synthesis of all five thiolated nucleosides present in tRNA from Salmonella enterica serovar Typhimurium. J. Bacteriol. 184, 6830-6835
24. Waterman, D. G., Ortiz-Lombardía, M., Fogg, M. J., Koonin, E. V., and Antson, A. A. (2006) Crystal structure of Bacillus anthracis ThiI, a tRNAmodifying enzyme containing the predicted RNA-binding THUMP domain. J. Mol. Biol. 356, 97-110
25. Tanaka, Y., Yamagata, S., Kitago, Y., Yamada, Y., Chimnaronk, S., Yao, M., and Tanaka, I. (2009) Deduced RNA binding mechanism of ThiI based on structural and binding analyses of a minimal RNA ligand. RNA 15, 1498-1506
26. Lauhon, C. T., Erwin, W. M., and Ton, G. N. (2004) Substrate specificity for 4-thiouridine modification in Escherichia coli. J. Biol. Chem. 279, 23022-23029
27. You, D., Xu, T., Yao, F., Zhou, X., and Deng, Z. (2008) Direct evidence that ThiI is an ATP pyrophosphatase for the adenylation of uridine in 4-thiouridine biosynthesis. ChemBioChem 9, 1879-1882
28. Mueller, E. G., and Palenchar, P. M. (1999) Using genomic information to investigate the function of ThiI, an enzyme shared between thiamin and 4-thiouridine biosynthesis. Protein Sci. 8, 2424-2427
29. Palenchar, P. M., Buck, C. J., Cheng, H., Larson, T. J., and Mueller, E. G. (2000) Evidence that ThiI, an enzyme shared between thiamin and 4-thiouridine biosynthesis, may be a sulfurtransferase that proceeds through a persulfide intermediate. J. Biol. Chem. 275, 8283-8286
30. Wright, C. M., Christman, G. D., Snellinger, A. M., Johnston, M. V., and Mueller, E. G. (2006) Direct evidence for enzyme persulfide and disulfide intermediates during 4-thiouridine biosynthesis. Chem. Commun. 3104-3106
31. Kambampati, R., and Lauhon, C. T. (2000) Evidence for the transfer of sulfane sulfur from IscS to ThiI during the in vitro biosynthesis of 4-thiouridine in Escherichia coli tRNA. J. Biol. Chem. 275, 10727-10730
32. Wright, C. M., Palenchar, P. M., and Mueller, E. G. (2002) A paradigm for biological sulfur transfers via persulfide groups. A persulfide-disulfidethiol cycle in 4-thiouridine biosynthesis. Chem. Commun. 2708-2709
33. Mueller, E. G., Palenchar, P. M., and Buck, C. J. (2001) The role of the cysteine residues of ThiI in the generation of 4-thiouridine in tRNA. J. Biol. Chem. 276, 33588-33595
34. Webb, E., Claas, K., and Downs, D. M. (1997) Characterization of thiI, a new gene involved in thiazole biosynthesis in Salmonella typhimurium. J. Bacteriol. 179, 4399-4402
35. Martinez-Gomez, N. C., Palmer, L. D., Vivas, E., Roach, P. L., and Downs, D. M. (2011) The rhodanese domain of ThiI is both necessary and sufficient for synthesis of the thiazole moiety of thiamine in Salmonella enterica. J. Bacteriol. 193, 4582-4587
36. Taylor, S. V., Kelleher, N. L., Kinsland, C., Chiu, H. J., Costello, C. A., Backstrom, A. D., McLafferty, F. W., and Begley, T. P. (1998) Thiamin biosynthesis in Escherichia coli. Identification of ThiS thiocarboxylate Abstract: the immediate sulfur donor in the thiazole formation. J. Biol. Chem. 273, 16555-16560
37. Rajakovich, L. J., Tomlinson, J., and Dos Santos, P. C. (2012) Functional analysis of Bacillus subtilis genes involved in the biosynthesis of 4-thiouridine in tRNA. J. Bacteriol.
38. Park, J. H., Dorrestein, P. C., Zhai, H., Kinsland, C., McLafferty, F. W., and Begley, T. P. (2003) Biosynthesis of the thiazole moiety of thiamin pyrophosphate (vitamin B1). Biochemistry 42, 12430-12438
39. Bender, R. A. (2011) The danger of annotation by analogy. Most "thiI" genes play no role in thiamine biosynthesis. J. Bacteriol. 193, 4574-4575
40. Edmonds, C. G., Crain, P. F., Gupta, R., Hashizume, T., Hocart, C. H., Kowalak, J. A., Pomerantz, S. C., Stetter, K. O., and McCloskey, J. A. (1991) Post-transcriptional modification of tRNA in thermophilic archaea (Archaebacteria). J. Bacteriol. 173, 3138-3148
41. Best, A. N. (1978) Composition and characterization of tRNA from Methanococcus vannielii. J. Bacteriol. 133, 240-250
42. McCloskey, J. A., Graham, D. E., Zhou, S., Crain, P. F., Ibba, M., Konisky, J., Söll, D., and Olsen, G. J. (2001) Post-transcriptional modification in archaeal tRNAs. Identities and phylogenetic relations of nucleotides from mesophilic and hyperthermophilic Methanococcales. Nucleic Acids Res. 29, 4699-4706
43. opt), 23 °C) and Stetteria hydrogenophila (Topt, 95 °C). J. Bacteriol. 185, 5483-5490
44. Liu, Y., Beer, L. L., and Whitman, W. B. (2012) Sulfur metabolism in archaea reveals novel processes. Environ. Microbiol. 194, 4933-4940
45. Sauerwald, A., Zhu, W., Major, T. A., Roy, H., Palioura, S., Jahn, D., Whitman, W. B., Yates, J. R., 3rd, Ibba, M., and Söll, D. (2005) RNA-dependent cysteine biosynthesis in archaea. Science 307, 1969-1972
46. Liu, Y., Sieprawska-Lupa, M., Whitman, W. B., and White, R. H. (2010) Cysteine is not the sulfur source for iron-sulfur cluster and methionine biosynthesis in the methanogenic archaeon Methanococcus maripaludis. J. Biol. Chem. 285, 31923-31929
47. Whitman, W. B., Shieh, J., Sohn, S., Caras, D. S., and Premachandran, U. (1986) Isolation and characterization of 22 mesophilic methanococci. Syst. Appl. Microbiol. 7, 235-240
48. Gernhardt, P., Possot, O., Foglino, M., Sibold, L., and Klein, A. (1990) Construction of an integration vector for use in the archaebacterium Methanococcus voltae and expression of a eubacterial resistance gene. Mol. Gen. Genet. 221, 273-279
49. Lin, W., and Whitman, W. B. (2004) The importance of porE and porF in the anabolic pyruvate oxidoreductase of Methanococcus maripaludis. Arch. Microbiol. 181, 68-73
50. Tumbula, D. L., Makula, R. A., and Whitman, W. B. (1994) Transformation of Methanococcus maripaludis and identification of a PstI-like restriction system. FEMS Microbiol. Lett. 121, 309-314
51. Smith, P. K., Krohn, R. I., Hermanson, G. T., Mallia, A. K., Gartner, F. H., Provenzano, M. D., Fujimoto, E. K., Goeke, N. M., Olson, B. J., and Klenk, D. C. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76-85
52. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K. A., Tomita, M., Wanner, B. L., and Mori, H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants. The Keio collection. Mol. Syst. Biol. 2, 1-11
53. Gupta, R. (1995) in Archaea: A Laboratory Manual (Robb, F. T., Place, A. R., Sowers, K. R., Schreier, H. J., DasSarma, S., and Fleischmann, E. M., eds) pp. 119-131, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
54. Mesbah, M., Premachandran, U., and Whitman, W. B. (1989) Precise measurement of the G+C content of deoxyribonucleic acid by high performance liquid chromatography. Int. J. Syst. Bacteriol. 39, 159-167
55. Hudson, E. N., and Weber, G. (1973) Synthesis and characterization of two fluorescent sulfhydryl reagents. Biochemistry 12, 4154-4161
56. Liu, Y., Dos Santos, P. C., Zhu, X., Orlando, R., Dean, D. R., Söll, D., and Yuan, J. (2012) Catalytic mechanism of Sep-tRNA:Cys-tRNA synthase. Sulfur transfer is mediated by disulfide and persulfide. J. Biol. Chem. 287, 5426-5433
57. Hohn, M. J., Park, H. S., O'Donoghue, P., Schnitzbauer, M., and Söll, D. (2006) Emergence of the universal genetic code imprinted in an RNA record. Proc. Natl. Acad. Sci. U.S.A. 103, 18095-18100
58. Miranda, H. V., Nembhard, N., Su, D., Hepowit, N., Krause, D. J., Pritz, J. R., Phillips, C., Söll, D., and Maupin-Furlow, J. A. (2011) E1- and ubiquitin- like proteins provide a direct link between protein conjugation and sulfur transfer in archaea. Proc. Natl. Acad. Sci. U.S.A. 108, 4417-4422
59. Liu, Y., Beer, L. L., and Whitman, W. B. (2012) Methanogens. A window into ancient sulfur metabolism. Trends Microbiol. 20, 251-258
60. Iqbalsyah, T. M., Moutevelis, E., Warwicker, J., Errington, N., and Doig, A. J. (2006) The CXXC motif at the N terminus of an α-helical peptide. Protein Sci. 15, 1945-1950
61. Numata, T., Ikeuchi, Y., Fukai, S., Suzuki, T., and Nureki, O. (2006) Snapshots of tRNA sulfuration via an adenylated intermediate. Nature 442, 419-424
62. Kambampati, R., and Lauhon, C. T. (2003) MnmA and IscS are required for in vitro 2-thiouridine biosynthesis in Escherichia coli. Biochemistry 42, 1109-1117
63. Leigh, J. A. (1983) Levels of water-soluble vitamins in methanogenic and nonmethanogenic bacteria. Appl. Environ. Microbiol. 45, 800-803
64. Phillips, G., and de Crécy-Lagard, V. (2011) Biosynthesis and function of tRNA modifications in Archaea. Curr. Opin. Microbiol. 14, 335-341
65. Pomerantz, S. C., and McCloskey, J. A. (1990) Analysis of RNA hydrolysates by liquid chromatography-mass spectrometry. Methods Enzymol. 193, 796-824