Essentiality of threonylcarbamoyladenosine (t6A), a universal tRNA modification, in bacteria

Molecular Microbiology

Volumn 98, Issue 6, 2015, Pages 1199-1221

  Thiaville, Patrick C ^a,b   El Yacoubi, Basma ^a   Köhrer, Caroline ^c   Thiaville, Jennifer J ^a   Deutsch, Chris ^d   Iwata Reuyl, Dirk ^d   Bacusmo, Jo Marie ^a   Armengaud, Jean ^e   Bessho, Yoshitaka ^f,g   Wetzel, Collin ^h   Cao, Xiaoyu ^h   Limbach, Patrick A ^h   Rajbhandary, Uttam L ^c   de Crécy Lagard, Valérie ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d PORTLAND STATE UNIVERSITY   (United States)

^e DIF   (France)

^f RIKEN SPring 8 Center ^*  (Japan)

^g INSTITUTE OF PHYSICS   (Taiwan)

^h UNIVERSITY OF CINCINNATI   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESSENTIAL AMINO ACID; ISOLEUCINE TRANSFER RNA LIGASE; ISOLEUCINE TRANSFER RNA LYSIDINE SYNTHETASE; PROTEIN THREONYLCARBAMOYLADENOSINE; TRANSFER RNA; UNCLASSIFIED DRUG; ADENOSINE; AMINO ACID TRANSFER RNA LIGASE; BACTERIAL RNA; N(6)-(N-THREONYLCARBONYL)ADENOSINE;

AMINOACYLATION; ARTICLE; BACTERIAL STRAIN; DEINOCOCCUS RADIODURANS; ENZYME MODIFICATION; ESCHERICHIA COLI; EUKARYOTE; GENE IDENTIFICATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROKARYOTE; PROTEOMICS; RNA SYNTHESIS; RNA TRANSLATION; STREPTOCOCCUS MUTANS; STRESS; SYNECHOCYSTIS; THERMUS THERMOPHILUS; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; CONSERVED SEQUENCE; DEINOCOCCUS; GENETICS; METABOLISM; MOLECULAR GENETICS; PROKARYOTIC CELL; SACCHAROMYCES CEREVISIAE;

ADENOSINE; AMINO ACID SEQUENCE; AMINO ACYL-TRNA SYNTHETASES; AMINOACYLATION; CONSERVED SEQUENCE; DEINOCOCCUS; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; PROKARYOTIC CELLS; PROTEOMICS; RNA, BACTERIAL; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE;

EID: 84983135328     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.13209     Document Type: Article

References (113)

1. Agris, P.F., Vendeix, F.A.P., and Graham, W.D. (2007) tRNA's wobble decoding of the genome: 40 years of modification. J Mol Biol 366: 1-13.
2. Akerley, B.J., Rubin, E.J., Novick, V.L., Amaya, K., Judson, N., and Mekalanos, J.J. (2002) A genome-scale analysis for identification of genes required for growth or survival of Haemophilus influenzae. Proc Natl Acad Sci USA 99: 966-971.
3. Allali-Hassani, A., Campbell, T.L., Ho, A., Schertzer, J.W., and Brown, E.D. (2004) Probing the active site of YjeE: a vital Escherichia coli protein of unknown function. Biochem J 384: 577-584.
4. Alonso, J.M., Stepanova, A.N., Leisse, T.J., Kim, C.J., Chen, H., Shinn, P., etal. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
5. Arigoni, F., Talabot, F., Peitsch, M., Edgerton, M.D., Meldrum, E., Allet, E., etal. (1998) A genome-based approach for the identification of essential bacterial genes. Nat Biotechnol 16: 851-856.
6. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., etal. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006 0008.
7. Begley, U., Dyavaiah, M., Patil, A., Rooney, J.P., DiRenzo, D., Young, C.M., etal. (2007) Trm9-catalyzed tRNA modifications link translation to the DNA damage response. Mol Cell 28: 860-870.
8. de Berardinis, V., Vallenet, D., Castelli, V., Besnard, M., Pinet, A., Cruaud, C., etal. (2008) A complete collection of single-gene deletion mutants of Acinetobacter baylyi ADP1. Mol Syst Biol 4: 174.
9. Bergmiller, T., Pena-Miller, R., Boehm, A., and Ackermann, M. (2011) Single-cell time-lapse analysis of depletion of the universally conserved essential protein YgjD. BMC Microbiol 11: 118.
10. Bergmiller, T., Ackermann, M., and Silander, O.K. (2012) Patterns of evolutionary conservation of essential genes correlate with their compensability. PLoS Genet 8: e1002803.
11. Bitoun, J.P., Liao, S., Xie, G.G., Beatty, W.L., and Wen, Z.T. (2014) Deficiency of BrpB causes major defects in cell division, stress responses and biofilm formation by Streptococcus mutans. Microbiology 160: 67-78.
12. Blaby, I.K., Phillips, G., Blaby-Haas, C.E., Gulig, K.S., El Yacoubi, B., and de Crécy Lagard, V. (2010) Towards a systems approach in the genetic analysis of archaea: accelerating mutant construction and phenotypic analysis in Haloferax volcanii. Archaea 2010: 426239.
13. Bohlke, N., and Budisa, N. (2014) Sense codon emancipation for proteome-wide incorporation of noncanonical amino acids: rare isoleucine codon AUA as a target for genetic code expansion. FEMS Microbiol Lett 351: 133-144.
14. Bouthier de la Tour, C., Passot, F.M., Toueille, M., Mirabella, B., Guerin, P., Blanchard, L., etal. (2013) Comparative proteomics reveals key proteins recruited at the nucleoid of Deinococcus after irradiation-induced DNA damage. Proteomics 13: 3457-3469.
15. Campbell, T.L., Ederer, C.S., Allali-Hassani, A., and Brown, E.D. (2007) Isolation of the rstA gene as a multicopy suppressor of YjeE, an essential ATPase of unknown function in Escherichia coli. J Bacteriol 189: 3318-3321.
16. Carvalho, P.C., Fischer, J.S., Xu, T., Yates, J.R., 3rd, and Barbosa, V.C. (2012) PatternLab: from mass spectra to label-free differential shotgun proteomics. Curr Protoc Bioinformatics Chapter 13: Unit13 19.
17. Caspi, R., Altman, T., Billington, R., Dreher, K., Foerster, H., Fulcher, C.A., etal. (2014) The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases. Nucleic Acids Res 42: D459-D471.
18. Chan, C.T.Y., Pang, Y.L.J., Deng, W., Babu, I.R., Dyavaiah, M., Begley, T.J., and Dedon, P.C. (2012) Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins. Nat Commun 3: 937.
19. Chao, M.C., Pritchard, J.R., Zhang, Y.J., Rubin, E.J., Livny, J., Davis, B.M., and Waldor, M.K. (2013) High-resolution definition of the Vibrio cholerae essential gene set with hidden Markov model-based analyses of transposon-insertion sequencing data. Nucleic Acids Res 41: 9033-9048.
20. Chaudhuri, R.R., Allen, A.G., Owen, P.J., Shalom, G., Stone, K., Harrison, M., etal. (2009) Comprehensive identification of essential Staphylococcus aureus genes using transposon-mediated differential hybridisation (TMDH). BMC Genomics 10: 291.
21. Christen, B., Abeliuk, E., Collier, J.M., Kalogeraki, V.S., Passarelli, B., Coller, J.A., etal. (2011) The essential genome of a bacterium. Mol Syst Biol 7: 528.
22. 6A modification of tRNAs. Nucleic Acids Res 39: 6148-6160.
23. Dedon, P.C., and Begley, T.J. (2014) A system of RNA modifications and biased codon use controls cellular stress response at the level of translation. Chem Res Toxicol 27: 330-337.
24. 6A), a universal tRNA nucleoside. J Biol Chem 287: 13666-13673.
25. Dreyfus, M., and Heurgue-Hamard, V. (2011) Termination troubles in Escherichia coli K12. Mol Microbiol 79: 288-291.
26. Dybvig, K., Lao, P., Jordan, D.S., and Simmons, W.L. (2010) Fewer essential genes in mycoplasmas than previous studies suggest. FEMS Microbiol Lett 311: 51-55.
27. El Yacoubi, B., Lyons, B., Cruz, Y., Reddy, R., Nordin, B., Agnelli, F., etal. (2009) The universal YrdC/Sua5 family is required for the formation of threonylcarbamoyladenosine in tRNA. Nucleic Acids Res 37: 2894-2909.
28. El Yacoubi, B., Hatin, I., Deutsch, C., Kahveci, T., Rousset, J.P., Iwata-Reuyl, D., etal. (2011) A role for the universal Kae1/Qri7/YgjD (COG0533) family in tRNA modification. EMBO J 30: 882-893.
29. El Yacoubi, B., Bailly, M., and de Crécy-Lagard, V. (2012) Biosynthesis and function of posttranscriptional modifications of transfer RNAs. Annu Rev Genet 46: 69-95.
30. Freiberg, C., Wieland, B., Spaltmann, F., Ehlert, K., Brotz, H., and Labischinski, H. (2001) Identification of novel essential Escherichia coli genes conserved among pathogenic bacteria. J Mol Microbiol Biotechnol 3: 483-489.
31. French, C.T., Lao, P., Loraine, A.E., Matthews, B.T., Yu, H., and Dybvig, K. (2008) Large-scale transposon mutagenesis of Mycoplasma pulmonis. Mol Microbiol 69: 67-76.
32. Gallagher, L.A., Ramage, E., Jacobs, M.A., Kaul, R., Brittnacher, M., and Manoil, C. (2007) A comprehensive transposon mutant library of Francisella novicida, a bioweapon surrogate. Proc Natl Acad Sci USA 104: 1009-1014.
33. Gallagher, L.A., Ramage, E., Patrapuvich, R., Weiss, E., Brittnacher, M., and Manoil, C. (2013) Sequence-defined transposon mutant library of Burkholderia thailandensis. MBio 4: e604-e613.
34. Gerdes, S., El Yacoubi, B., Bailly, M., Blaby, I.K., Blaby-Haas, C.E., Jeanguenin, L., etal. (2011) Synergistic use of plant-prokaryote comparative genomics for functional annotations. BMC Genomics 12: S2.
35. Giegé, R., and Lapointe, J. (2009) Transfer RNA aminoacylation and modified nucleosides. In DNA and RNA Modification Enzymes: Comparative Structure, Mechanism, Functions, Cellular Interactions and Evolution. Grosjean, H. (ed.). Austin, TX: Landes Bioscience, pp. 475-492.
36. Giegé, R., Sissler, M., and Florentz, C. (1998) Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res 26: 5017-5035.
37. Glass, J.I., Assad-Garcia, N., Alperovich, N., Yooseph, S., Lewis, M.R., Maruf, M., etal. (2006) Essential genes of a minimal bacterium. Proc Natl Acad Sci USA 103: 425-430.
38. Grosjean, H., Breton, M., Sirand-Pugnet, P., Tardy, F., Thiaucourt, F., Citti, C., etal. (2014) Predicting the minimal translation apparatus: lessons from the reductive evolution of mollicutes. PLoS Genet 10: e1004363.
39. Gu, C., Begley, T.J., and Dedon, P.C. (2014) tRNA modifications regulate translation during cellular stress. FEBS Lett 588: 4287-4296.
40. Handford, J.I., Ize, B., Buchanan, G., Butland, G.P., Greenblatt, J., Emili, A., and Palmer, T. (2009) Conserved network of proteins essential for bacterial viability. J Bacteriol 191: 4732-4749.
41. Hartmann, E.M., Allain, F., Gaillard, J.C., Pible, O., and Armengaud, J. (2014) Taking the shortcut for high-throughput shotgun proteomic analysis of bacteria. Methods Mol Biol 1197: 275-285.
42. Hashimoto, C., Sakaguchi, K., Taniguchi, Y., Honda, H., Oshima, T., Ogasawara, N., and Kato, J. (2011) Effects on transcription of mutations in ygjD, yeaZ, and yjeE genes, which are involved in a universal tRNA modification in Escherichia coli. J Bacteriol 193: 6075-6079.
43. Hashimoto, C., Hashimoto, M., Honda, H., and Kato, J.I. (2013) Effects on IS1 transposition frequency of a mutation in the ygjD gene involved in an essential tRNA modification in Escherichia coli. FEMS Microbiol Lett 347: 140-148.
44. Hashimoto, Y., Yano, T., Kuramitsu, S., and Kagamiyama, H. (2001) Disruption of Thermus thermophilus genes by homologous recombination using a thermostable kanamycin-resistant marker. FEBS Lett 506: 231-234.
45. Hunt, A., Rawlins, J.P., Thomaides, H.B., and Errington, J. (2006) Functional analysis of 11 putative essential genes in Bacillus subtilis. Microbiology 152: 2895-2907.
46. Ibba, M., Curnow, A.W., Bono, J., Rosa, P.A., Woese, C.R., and Söll, D. (1999) Archaeal aminoacyl-tRNA synthesis: unique determinants of a universal genetic code? Biol Bull 196: 335-337.
47. Ikeuchi, Y., Soma, A., Ote, T., Kato, J., Sekine, Y., and Suzuki, T. (2005) Molecular mechanism of lysidine synthesis that determines tRNA identity and codon recognition. Mol Cell 19: 235-246.
48. Ikeuchi, Y., Kimura, S., Numata, T., Nakamura, D., Yokogawa, T., Ogata, T., etal. (2010) Agmatine-conjugated cytidine in a tRNA anticodon is essential for AUA decoding in archaea. Nat Chem Biol 6: 277-282.
49. Jacobs, M.A., Alwood, A., Thaipisuttikul, I., Spencer, D., Haugen, E., Ernst, S., etal. (2003) Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 100: 14339-14344.
50. Jühling, F., Mörl, M., Hartmann, R.K., Sprinzl, M., Stadler, P.F., and Pütz, J. (2009) tRNAdb 2009: compilation of tRNA sequences and tRNA genes. Nucleic Acids Res 37: D159-D162.
51. Kaczanowska, M., and Rydén-Aulin, M. (2005) The YrdC protein - a putative ribosome maturation factor. Biochim Biophys Acta 1727: 87-96.
52. Kaczanowska, M., and Ryden-Aulin, M. (2004) Temperature sensitivity caused by mutant Release Factor 1 is suppressed by mutations that affect 16S rRNA Maturation. J Bacteriol 186: 3046-3055.
53. Kamp, H.D., Patimalla-Dipali, B., Lazinski, D.W., Wallace-Gadsden, F., and Camilli, A. (2013) Gene fitness landscapes of Vibrio cholerae at important stages of its life cycle. PLoS Pathog 9: e1003800.
54. Katz, C., Cohen-Or, I., Gophna, U., and Ron, E.Z. (2010) The ubiquitous conserved glycopeptidase Gcp prevents accumulation of toxic glycated proteins. MBio 1: e00195-10.
55. Kelley, L.A., and Sternberg, M.J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
56. Kim, D.U., Hayles, J., Kim, D., Wood, V., Park, H.O., Won, M., etal. (2010) Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe. Nature Biotechnol 28: 617-623.
57. Kisseleva-Romanova, E., Lopreiato, R., Baudin-Baillieu, A., Rousselle, J.C., Ilan, L., Hofmann, K., etal. (2006) Yeast homolog of a cancer-testis antigen defines a new transcription complex. EMBO J 25: 3576-3585.
58. Kitagawa, M., Ara, T., Arifuzzaman, M., Ioka-Nakamichi, T., Inamoto, E., Toyonaga, H., and Mori, H. (2006) Complete set of ORF clones of Escherichia coli ASKA library (A Complete Set of E. coli K-12 ORF Archive): unique resources for biological research. DNA Res 12: 291-299.
59. Klekamp, M.S., and Weil, P.A. (1982) Specific transcription of homologous class III genes in yeast-soluble cell-free extracts. J Biol Chem 257: 8432-8441.
60. Kobayashi, K., Ehrlich, S.D., Albertini, A., Amati, G., Andersen, K.K., Arnaud, M., etal. (2003) Essential Bacillus subtilis genes. Proc Natl Acad Sci USA 100: 4678-4683.
61. Köhrer, C., Srinivasan, G., Mandal, D., Mallick, B., Ghosh, Z., Chakrabarti, J., and RajBhandary, U.L. (2008) Identification and characterization of a tRNA decoding the rare AUA codon in Haloarcula marismortui. RNA 14: 117-126.
62. Langridge, G.C., Phan, M.D., Turner, D.J., Perkins, T.T., Parts, L., Haase, J., etal. (2009) Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Res 19: 2308-2316.
63. 6A) biosynthesis: isolation and characterization of the intermediate threonylcarbamoyl-AMP. Biochemistry 51: 8950-8963.
64. Lerner, C.G., Hajduk, P.J., Wagner, R., Wagenaar, F.L., Woodall, C., Gu, Y.G., etal. (2007) From bacterial genomes to novel antibacterial agents: discovery, characterization, and antibacterial activity of compounds that bind to HI0065 (YjeE) from Haemophilus influenzae. Chem Biol Drug Des 69: 395-404.
65. Lin, C.A., Ellis, S.R., and True, H.L. (2009) The Sua5 protein is essential for normal translational regulation in yeast. Mol Cell Biol 30: 354-363.
66. Makarova, K.S., Aravind, L., Wolf, Y.I., Tatusov, R.L., Minton, K.W., Koonin, E.V., and Daly, M.J. (2001) Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol Mol Biol Rev 65: 44-79.
67. Mandal, D., Kohrer, C., Su, D., Russell, S.P., Krivos, K., Castleberry, C.M., etal. (2010) Agmatidine, a modified cytidine in the anticodon of archaeal tRNA(Ile), base pairs with adenosine but not with guanosine. Proc Natl Acad Sci USA 107: 2872-2877.
68. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
69. Msadek, T. (2009) Grasping at shadows: revealing the elusive nature of essential genes. J Bacteriol 191: 4701-4704.
70. Muramatsu, T., Nishikawa, K., Nemoto, F., Kuchino, Y., Nishimura, S., Miyazawa, T., and Yokoyama, S. (1988a) Codon and amino-acid specificities of a transfer RNA are both converted by a single post-transcriptional modification. Nature 336: 179-181.
71. Muramatsu, T., Yokoyama, S., Horie, N., Matsuda, A., Ueda, T., Yamaizumi, Z., etal. (1988b) A novel lysine-substituted nucleoside in the first position of the anticodon of minor isoleucine tRNA from Escherichia coli. J Biol Chem 263: 9261-9267.
72. Na, J.G., Pinto, I., and Hampsey, M. (1992) Isolation and characterization of SUA5, a novel gene required for normal growth in Saccharomyces cerevisiae. Genetics 131: 791-801.
73. Nakanishi, K., Fukai, S., Ikeuchi, Y., Soma, A., Sekine, Y., Suzuki, T., and Nureki, O. (2005) Structural basis for lysidine formation by ATP pyrophosphatase accompanied by a lysine-specific loop and a tRNA-recognition domain. Proc Natl Acad Sci USA 102: 7487-7492.
74. Naor, A., Thiaville, P.C., Altman-Price, N., Cohen-Or, I., Allers, T., de Crécy-Lagard, V., and Gophna, U. (2012) A genetic investigation of the KEOPS complex in halophilic Archaea. PLoS ONE 7: e43013.
75. Nedialkova, D.D., and Leidel, S.A. (2015) Modified nucleosides in the tRNA anticodon accelerate decoding to maintain protein solubility. Cell.
76. Nureki, O., Niimi, T., Muramatsu, T., Kanno, H., Kohno, T., Florentz, C., etal. (1994) Molecular recognition of the identity-determinant set of isoleucine transfer RNA from Escherichia coli. J Mol Biol 236: 710-724.
77. Oberto, J., Breuil, N., Hecker, A., Farina, F., Brochier-Armanet, C., Culetto, E., and Forterre, P. (2009) Qri7/OSGEPL, the mitochondrial version of the universal Kae1/YgjD protein, is essential for mitochondrial genome maintenance. Nuceic Acids Res 37: 5343-5352.
78. Ohtani, N., Tomita, M., and Itaya, M. (2010) An extreme thermophile, Thermus thermophilus, is a polyploid Bacterium. J Bacteriol 192: 5499-5505.
79. Onodera, T., Satoh, K., Ohta, T., and Narumi, I. (2013) Deinococcus radiodurans YgjD and YeaZ are involved in the repair of DNA cross-links. Extremophiles 17: 171-179.
80. Osawa, T., Kimura, S., Terasaka, N., Inanaga, H., Suzuki, T., and Numata, T. (2011) Structural basis of tRNA agmatinylation essential for AUA codon decoding. Nat Struct Mol Biol 18: 1275-1280.
81. Patel, B.A., Moreau, M., Widom, J., Chen, H., Yin, L., Hua, Y., and Crane, B.R. (2009) Endogenous nitric oxide regulates the recovery of the radiation-resistant bacterium Deinococcus radiodurans from exposure to UV light. Proc Natl Acad Sci USA 106: 18183-18188.
82. Patil, A., Chan, C.T., Dyavaiah, M., Rooney, J.P., Dedon, P.C., and Begley, T.J. (2012a) Translational infidelity-induced protein stress results from a deficiency in Trm9-catalyzed tRNA modifications. RNA Biol 9: 990-1001.
83. Patil, A., Dyavaiah, M., Joseph, F., Rooney, J.P., Chan, C.T., Dedon, P.C., and Begley, T.J. (2012b) Increased tRNA modification and gene-specific codon usage regulate cell cycle progression during the DNA damage response. Cell Cycle 11: 3656-3665.
84. 6A tRNA modification in Archaea and Eukarya. Nucleic Acids Res 41: 1953-1964.
85. Pomerantz, S.C., and McCloskey, J.A. (1990) Analysis of RNA hydrolyzates by liquid chromatography-mass spectrometry. Methods Enzymol 193: 796-824.
86. Puri, P., Wetzel, C., Saffert, P., Gaston, K.W., Russell, S.P., Cordero Varela, J.A., etal. (2014) Systematic identification of tRNAome and its dynamics in Lactococcus lactis. Mol Microbiol 93: 944-956.
87. Racher, K.I., Kalmar, G.B., and Borgford, T.J. (1991) Expression and characterization of a recombinant yeast isoleucyl-tRNA synthetase. J Biol Chem 266: 17158-17164.
88. Ramos, J.L., Martinez-Bueno, M., Molina-Henares, A.J., Teran, W., Watanabe, K., Zhang, X., etal. (2005) The TetR family of transcriptional repressors. Microbiol Mol Biol Rev 69: 326-356.
89. Rezgui, V.A.N., Tyagi, K., Ranjan, N., Konevega, A.L., Mittelstaet, J., Rodnina, M.V., etal. (2013) tRNA tKUUU, tQUUG, and tEUUC wobble position modifications fine-tune protein translation by promoting ribosome A-site binding. Proc Natl Acad Sci USA 110: 12289-12294.
90. Russell, S.P., and Limbach, P.A. (2013) Evaluating the reproducibility of quantifying modified nucleosides from ribonucleic acids by LC-UV-MS. J Chromatogr B Analyt Technol Biomed Life Sci 923-924: 74-82.
91. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
92. Sarmiento, F., MrÃzek, J., and Whitman, W.B. (2013) Genome-scale analysis of gene function in the hydrogenotrophic methanogenic archaeon Methanococcus maripaludis. Proc Natl Acad Sci USA 110: 4726-4731.
93. Sassanfar, M., Kranz, J.E., Gallant, P., Schimmel, P., and Shiba, K. (1996) A eubacterial Mycobacterium tuberculosis tRNA synthetase is eukaryote-like and resistant to a eubacterial-specific antisynthetase drug. Biochemistry 35: 9995-10003.
94. Senger, B., Auxilien, S., Englisch, U., Cramer, F., and Fasiolo, F. (1997) The modified wobble base inosine in yeast tRNAIle is a positive determinant for aminoacylation by isoleucyl-tRNA synthetase. Biochemistry 36: 8269-8275.
95. Serina, S., Nozza, F., Nicastro, G., Faggioni, F., Mottl, H., Deho, G., and Polissi, A. (2004) Scanning the Escherichia coli chromosome by random transposon mutagenesis and multiple phenotypic screening. Res Microbiol 155: 692-701.
96. Shepherd, J., and Ibba, M. (2014) Relaxed substrate specificity leads to extensive tRNA Mischarging by Streptococcus pneumoniae class I and Class II aminoacyl-tRNA synthetases. MBio 5: 01656-14.
97. Soma, A., Ikeuchi, Y., Kanemasa, S., Kobayashi, K., Ogasawara, N., Ote, T., etal. (2003) An RNA-modifying enzyme that governs both the codon and amino acid specificities of isoleucine tRNA. Mol Cell 12: 689-698.
98. Spirek, M., Benko, Z., Carnecka, M., Rumpf, C., Cipak, L., Batova, M., etal. (2010) S. pombe genome deletion project: an update. Cell Cycle 9: 2399-2402.
99. Stothard, P. (2000) The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 28: 1102, 1104.
100. Suzuki, T., and Miyauchi, K. (2010) Discovery and characterization of tRNAIle lysidine synthetase (TilS). FEBS Lett 584: 272-277.
101. Taniguchi, T., Miyauchi, K., Nakane, D., Miyata, M., Muto, A., Nishimura, S., and Suzuki, T. (2013) Decoding system for the AUA codon by tRNAIle with the UAU anticodon in Mycoplasma mobile. Nucleic Acids Res 41: 2621-2631.
102. Thiaville, P.C., El Yacoubi, B., Perrochia, L., Hecker, A., Prigent, M., Thiaville, J.J., etal. (2014a) Cross kingdom functional conservation of the core universally conserved threonylcarbamoyladenosine tRNA synthesis enzymes. Eukaryot Cell 13: 1222-1231.
103. 6A), a universal modification of tRNA. RNA Biol 11: 1529-1539.
104. Tumu, S., Patil, A., Towns, W., Dyavaiah, M., and Begley, T.J. (2012) The gene-specific codon counting database: a genome-based catalog of one-, two-, three-, four- and five-codon combinations present in Saccharomyces cerevisiae genes. Database (Oxford) 2012: bas002.
105. Wan, L.C.K., Mao, D.Y.L., Neculai, D., Strecker, J., Chiovitti, D., Kurinov, I., etal. (2013) Reconstitution and characterization of eukaryotic N6-threonylcarbamoylation of tRNA using a minimal enzyme system. Nucleic Acids Res 41: 6332-6346.
106. Wattam, A.R., Abraham, D., Dalay, O., Disz, T.L., Driscoll, T., Gabbard, J.L., etal. (2014) PATRIC, the bacterial bioinformatics database and analysis resource. Nucleic Acids Res 42: D581-D591.
107. Wetzel, C., and Limbach, P.A. (2013) The global identification of tRNA isoacceptors by targeted tandem mass spectrometry. Analyst 138: 6063-6072.
108. Winzeler, E.A. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285: 901-906.
109. Woese, C.R., Olsen, G.J., Ibba, M., and Soll, D. (2000) Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol Mol Biol Rev 64: 202-236.
110. Wower, I.K., Wower, J., and Zimmermann, R.A. (1998) Ribosomal protein L27 participates in both 50 S subunit assembly and the peptidyl transferase reaction. J Biol Chem 273: 19847-19852.
111. Zhang, W., Collinet, B., Graille, M., Daugeron, M.C., Lazar, N., Libri, D., etal. (2015) Crystal structures of the Gon7/Pcc1 and Bud32/Cgi121 complexes provide a model for the complete yeast KEOPS complex. Nucleic Acids Res 43: 3358-3372.
112. Zhou, J., and Rudd, K.E. (2013) EcoGene 3.0. Nucleic Acids Res 41: D613-D624.
113. Zuther, E., Schubert, H., and Hagemann, M. (1998) Mutation of a gene encoding a putative glycoprotease leads to reduced salt tolerance, altered pigmentation, and cyanophycin accumulation in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 180: 1715-1722.