Chapter 9 : Features of Aminoacyl-tRNA Synthesis Unique to

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This chapter discusses four unique aspects of archaeal aa-tRNA formation that led to a much deeper understanding of this process not only in the , but in all domains of life. The topics are: (i) processing of half-tRNA genes to mature tRNA in , (ii) RNA-dependent cysteine synthesis in methanogens, (iii) pyrrolysyl-tRNA formation in the , and (iv) glutaminyl- tRNA synthesis in archaea. The bulge-helix-bulge (BHB) motifs postulated to form at the intron-exon junctions of archaeal tRNAs show divergence from the canonical structure. Once mature tRNA has been generated each tRNA species needs to be acylated (charged) with the correct amino acid. This is primarily achieved by the direct attachment of an amino acid to the corresponding tRNA by an aminoacyl-tRNA synthetase. However, since many organisms lack the complete set of 20 aminoacyl-tRNA synthetases (aaRSs), many biochemical, genetic, and genomic studies revealed the existence of an essential indirect two-step pathway that also provides correctly charged aa-tRNA. The aminoacyl-tRNA synthetases are an ancient family of enzymes that esterify an amino acid to the 3’ end of the cognate tRNA species. The current understanding of the Glu-tRNA amidotransferase GatDE is discussed. Discovery of the tRNA-dependent cysteine biosynthetic route in may have implications that reach far beyond the only problem of the formation of Cys-tRNA in three methanogenic archaea. The are an exception among the methanogens, as they are able to use compounds like methanol, methylated thiols, and methylamines as energy sources.

Citation: Polycarpo C, Sheppard K, Randau L, Ambrogelly A, Cardoso A, Fukai S, Herring S, Hohn M, Nakamura Y, Oshikane H, Palioura S, Salazar J, Yuan J, Nureki O, Söll D. 2007. Features of Aminoacyl-tRNA Synthesis Unique to , p 198-208. In Cavicchioli R (ed), Archaea. ASM Press, Washington, DC. doi: 10.1128/9781555815516.ch9
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Image of Figure 1.
Figure 1.

Schematic representation of and Conventional "-splicing involves a splicing endonuclease that recognizes and cleaves a bulge-helix-bulge RNA motif in the pre-tRNA leading to the excision of the intron (black). An RNA ligase generates the mature tRNA (gray). The unique of tRNA observed in requires the annealing of intervening reverse complementary sequences (black) found in the primary transcripts of a 5ʹ-tRNA half-gene and a 3ʹ-tRNA half-gene. Noncanonical splicing motifs are accommodated at the junctions and recognized by the splicing endonuclease.

Citation: Polycarpo C, Sheppard K, Randau L, Ambrogelly A, Cardoso A, Fukai S, Herring S, Hohn M, Nakamura Y, Oshikane H, Palioura S, Salazar J, Yuan J, Nureki O, Söll D. 2007. Features of Aminoacyl-tRNA Synthesis Unique to , p 198-208. In Cavicchioli R (ed), Archaea. ASM Press, Washington, DC. doi: 10.1128/9781555815516.ch9
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Image of Figure 2.
Figure 2.

Schematic representations of indirect pathways for aminoacyl-tRNA formation. (A) Route of Cys-tRNA formation in , and structures of phosphoserine and cysteine. (B) The indirect route for Gln-tRNA formation.

Citation: Polycarpo C, Sheppard K, Randau L, Ambrogelly A, Cardoso A, Fukai S, Herring S, Hohn M, Nakamura Y, Oshikane H, Palioura S, Salazar J, Yuan J, Nureki O, Söll D. 2007. Features of Aminoacyl-tRNA Synthesis Unique to , p 198-208. In Cavicchioli R (ed), Archaea. ASM Press, Washington, DC. doi: 10.1128/9781555815516.ch9
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Image of Figure 3.
Figure 3.

Schematic representation of the pyrrolysyl-tRNA formation by PylRS and structures of pyrrolysine and lysine.

Citation: Polycarpo C, Sheppard K, Randau L, Ambrogelly A, Cardoso A, Fukai S, Herring S, Hohn M, Nakamura Y, Oshikane H, Palioura S, Salazar J, Yuan J, Nureki O, Söll D. 2007. Features of Aminoacyl-tRNA Synthesis Unique to , p 198-208. In Cavicchioli R (ed), Archaea. ASM Press, Washington, DC. doi: 10.1128/9781555815516.ch9
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1. Abelson, J.,, C. R. Trotta, and, H. Li. 1998. tRNA splicing. J. Biol. Chem. 273 : 1268512688.
2. Ambrogelly, A.,, S. Kamtekar,, A. Sauerwald,, B. Ruan,, D. Tumbula-Hansen,, D. Kennedy,, I. Ahel, and, D. Söll. 2004. Cys-tRNA Cys formation and cysteine biosynthesis in Methanocal-dococcus jannaschii: two faces of the same problem? Cell. Mol. Life Sci. 61 : 24372445.
3. An, S., and, K. Musier-Forsyth. 2004. Trans-editing of Cys-tRNA Pro by Haemophilus influenzae YbaK protein. J. Biol. Chem. 279 : 4235942362.
4. Blight, S. K.,, R. C. Larue,, A. Mahapatra,, D. G. Longstaff,, E. Chang,, G. Zhao,, P. T. Kang,, K. B. Greenchurch,, M. K. Chan, and, J. A. Krzycki. 2004. Direct charging of tRNACUA with pyrrolysine in vitro and in vivo. Nature 431 : 333335.
5. Böck, A.,, M. Thanbichler,, M. Rother, and, A. Resch. 2005. Selenocysteine, p. 320327. In M. Ibba,, C. S. Francklyn,, S. Cusack (ed.), Aminoacyl-tRNA Synthetases. Landes Bioscience, Georgetown, Tex.
6. Boone, D. R.,, W. B. Whitman, and, P. Rouvière. 1993. Diversity and taxonomy of methanogens, p. 3580. In J. G. Ferry (ed.), Methanogenesis. Chapman & Hall, New York, N.Y.
7. Brooks, D. J., and, J. R. Fresco. 2002. Increased frequency of cysteine, tyrosine and phenylalanine residues since the last universal ancestor. Mol. Cell. Proteomics 1 : 125131.
8. Burkard, U.,, I. Willis, and, D. Söll. 1988. Processing of histidine transfer RNA precursors: abnormal cleavage site for RNase P. J. Biol. Chem. 263 : 24472451.
9. Calvin, K.,, M. D. Hall,, F. Xu,, S. Xue, and, H. Li. 2005. Structural characterization of the catalytic subunit of a novel RNA splicing endonuclease. J. Mol. Biol. 353 : 952960.
10. Connolly, S. A.,, A. E. Rosen,, K. Musier-Forsyth, and, C. S. Francklyn. 2004. G-1:C73 recognition by an arginine cluster in the active site of Escherichia coli histidyl-tRNA synthetase. Biochemistry 43 : 962969.
11. Cooley, L.,, B. Appel, and, D. Söil, D. 1982. Post-transcriptional nucleotide addition is responsible for the maturation of the 5ʹ-terminus of histidine tRNA. Proc. Natl. Acad. Sci. USA 79 : 64756479.
12. Curnow, A. W.,, K. Hong,, R. Yuan,, S. Martins,, W. Winkler,, T. M. Henkin, and, D. Söil. 1997. Glu-tRNA Gln amidotrans-ferase: a novel heterotrimeric enzyme required for correct decoding of glutamine codons during translation. Proc. Natl. Acad. Sci. USA 94 : 1181911826.
13. Curnow, A. W.,, M. Ibba, and, D. Soil. 1996. tRNA-dependent asparagine formation. Nature 382 : 589590.
14. Feng, L.,, K. Sheppard,, D. Tumbula-Hansen, and, D. Söil. 2005. Gln-tRNA Gln formation from Glu-tRNA Gln requires cooperation of an asparaginase and a Glu-tRNA Gln kinase. J. Biol. Chem. 280 : 81508155.
15. Furter, R. 1998. Expansion of the genetic code: site-directed p-fluoro-phenylalanine incorporation in Escherichia coli. Protein Sci. 7 : 419426.
16. Galagan, J. E.,, C. Nusbaum,, A. Roy,, M. G. Endrizzi,, P. Macdonald,, W. FitzHugh,, S. Calvo,, R. Engels,, S. Smirnov,, D. Atnoor,, A. Brown,, N. Allen,, J. Naylor,, N. Stange-Thomann,, K. DeArellano,, R. Johnson,, L. Linton,, P. McEwan,, K. McKernan,, J. Talamas,, A. Tirrell,, W. Ye,, A. Zimmer,, R. D. Barber, I. Cann,, D. E. Graham,, D. A. Grahame,, A. M. Guss,, R. Hedderich,, C. Ingram-Smith,, H. C. Kuettner,, J. A. Krzycki,, J. A. Leigh,, W. Li,, J. Liu,, B. Mukhopadhyay,, J. N. Reeve,, K. Smith,, T. A. Springer,, L. A. Umayam,, O. White,, R. H. White,, E. Conway de Macario,, J. G. Ferry,, K. F. Jarrell,, H. Jing,, A. J. Macario,, I. Paulsen,, M. Pritchett,, K. R. Sowers,, R. V. Swanson,, S. H. Zinder,, E. Lander,, W. W Metcalf, and, B. Birren. 2002. The genome of M. acetivorans reveals extensive metabolic and physiological diversity. Genome Res. 12 : 532542.
17. Goodchild, A.,, N. F. Saunders,, H. Ertan,, M. Raftery,, M. Guilhaus,, P. M. Curmi, and, R. Cavicchioli. 2004. A proteomic determination of cold adaptation in the antarctic archaeon, Methanococcoides burtonii. Mol. Microbiol. 53 : 309321.
18. Gopalan, V.,, A. Vioque, and, S. Altman. 2002. RNase P: variations and uses. J. Biol. Chem. 277 : 67596762.
19. Graham, D. E.,, H. Xu, and, R. H. White. 2002. Identification of coenzyme M biosynthetic phosphosulfolactate synthase. A new family of sulfonate-biosynthesizing enzymes. J. Biol. Chem. 277 : 1342113429.
20. Gu, W.,, J. E. Jackman,, A. J. Lohan,, M. W. Gray, and, E. M. Phizicky. 2003. tRNA His maturation: an essential yeast protein catalyzes addition of a guanine nucleotide to the 5- end of tRNAHis. Genes Dev. 17 : 28892901.
21. Hain, J.,, W. D. Reiter,, U. Hudepohl, and, W. Zillig. 1992. Elements of an archaeal promoter defined by mutational analysis. Nucleic Acids Res. 20 : 54235428.
22. Hao, B.,, W. Gong,, T. K. Ferguson,, C. M. James,, J. A. Krzycki, and, M. K. Chan. 2002. A new UAG-encoded residue in the structure of a methanogen methyltransferase. Science 296 : 14621466.
23. Hao, B.,, G. Zhao,, P. T. Kang,, J. A. Soares,, T. K. Ferguson,, J. Gallucci,, J. A. Krzycki, and, M. K. Chan. 2004. Reactivity and chemical synthesis of L-pyrrolysine-the 22 nd genetically encoded amino acid.. Chem. Biol. 11 : 13171324.
24. Hendrickson, T. L., and, P. Schimmel. 2003. Transfer RNA-dependent amino acid discrimination by aminoacyl-tRNA synthetases, p. 3464. In J. Lapointe and, L. Brakier-Gingras (eds.), Translation Mechanisms. Kluwer Academic Plenum Publishers, Dordrecht, The Netherlands.
25. Ibba, M.,, S. Morgan,, A. W. Curnow,, D. R. Pridmore,, U. C. Vothknecht,, W. Gardner,, W. Lin,, C. R. Woese, and, D. Söil. 1997. A euryarchaeal lysyl-tRNA synthetase: resemblance to class I synthetases. Science 278 : 11191122.
26. Ibba, M., and, D. Söll. 2000. Aminoacyl-tRNA synthesis. Annu. Rev. Biochem. 69 : 617650.
27. Ibba, M., and, D. Söll. 2001. The renaissance of aminoacyl-tRNA synthesis. EMBO Rep. 2 : 382387.
28. Ibba, M., and, D. Söll. 2004. Aminoacyl-tRNAs: setting the limits of the genetic code. Genes Dev. 18 : 731738.
29. James, C. M.,, T. K. Ferguson,, J. F. Leykam, and, J. A. Krzycki. 2001. The amber codon in the gene encoding the mono-methylamine methyltransferase isolated from Methanosarcina barkeri is translated as a sense codon. J. Biol. Chem. 276 : 3425234258.
30. Klug, G.,, E. Evguenieva-Hackenberg,, A. D. Omer,, P. P. Dennis, and, A. Marchfelder. 2007. RNA processing. p. 158174. In R. Cavicchioli (ed.), Archaea: Molecular and Cellular Biology. ASM Press, Washington, D.C.
31. Köhrer, C.,, E. L. Sullivan, and, U. L RajBhandary. 2004. Complete set of orthogonal21 st aminoacyl-tRNA synthetase-amber, ochre and opal suppressor tRNA pairs: concomitant suppression of three different termination codons in an mRNA in mammalian cells. Nucleic Acids Res. 32 : 62006211.
32. Li, H.,, C. R. Trotta, and, J. Abelson. 1998. Crystal structure and evolution of a transfer RNA splicing enzyme. Science 280 : 279284.
33. Li, Y., and, S. Altman. 2004. In search of RNase P RNA from microbial genomes. RNA 10 : 15331540.
34. Marck, C., and, H. Grosjean. 2002. tRNomics: analysis of tRNA genes from 50 genomes of Eukarya, Archaea, and Bacteria reveals anticodon-sparing strategies and domain-specific features. RNA 8 : 11891232.
35. Marck, C., and, H. Grosjean. 2003. Identification of BHB splicing motifs in intron-containing tRNAs from 18 archaea: evolutionary implications. RNA 9 : 15161531.
36. McCloskey, J. A.,, D. E. Graham,, S. Zhou,, P. F. Crain,, M. Ibba,, J. Konisky,, D. Söll, and, G. J. Olsen. 2001. Post-transcriptional modification in archaeal tRNAs: identities and phylogenetic relations of nucleotides from mesophilic and hyperthermophilic Methanococcales. Nucleic Acids Res. 29 : 46994706.
37. Michelitsch, M. D., and, J. S. Weissman. 2000. A census of glutamine/asparaginerich regions: implications for their conserved function and the prediction of novel prions. Proc. Natl. Acad. Sci. USA 97 : 1191011915.
38. Min, B.,, J. T. Pelaschier,, D. E. Graham,, D. Tumbula-Hansen, and, D. Söll. 2002. Transfer RNA-dependent amino acid biosynthesis: an essential route to asparagine formation. Proc. Natl. Acad. Sci. USA 99 : 26782683.
39. Namy, O.,, J.-P. Rousset,, S. Napthine, and, I. Brierley. 2004. Re-programmed genetic decoding in cellular gene expression. Mol. Cell 13 : 157168.
40. OʹDonoghue, P.,, A. Sethi,, C. R. Woese, and, Z. A. Luthey-Schulten. 2005. The evolutionary history of Cys-tRNACys formation. Proc. Natl. Acad. Sci. USA 102 : 1900319008.
41. Oshikane, H.,, K. Sheppard,, S. Fukai,, Y. Nakamura,, R. Ishitani,, T. Numata,, R. L. Sherrer,, L. Feng,, E. Schmitt,, M. Panvert,, S. Blanquest,, Y. Mechulam,, D. Söll, and, O. Nureki. 2006. Structural basis of RNA-dependent recruitment of glutamine to the genetic code. Science 312 : 19501954.
42. Palmer, J. R., and, C. J. Daniels. 1995. In vivo definition of an archaeal promoter. J. Bacteriol. 177 : 18441849.
43. Polycarpo, C.,, A. Ambrogelly,, A. Bérubé,, S. M. Winbush,, J. A. McCloskey,, P. F. Crain,, J. L. Wood, and, D. Söll. 2004. An aminoacyl-tRNA synthetase that specifically activates pyrrolysine. Proc. Natl. Acad. Sci. USA 101 : 1245012454.
44. Polycarpo, C.,, A. Ambrogelly, and, B. Ruan,, D. Tumbula-Hansen,, S. F. Ataide,, R. Ishitani,, S. Yokoyama,, O. Nureki,, M. Ibba, and, D. Soil. 2003. Activation of the pyrrolysine suppressor tRNA requires formation of a ternary complex with class I and class II lysyl- tRNA synthetases. Mol. Cell 12 : 287294.
45. Randau, L.,, K. Calvin,, M. Hall,, J. Yuan,, H. Li, and, D. Söil. 2005. A heteromeric splicing endonuclease of Nanoarchaeum equitans cleaves non-canonical bulge-helix-bulge motifs of joined tRNA halves. Proc. Natl. Acad. Sci. USA 102 : 1793417939.
46. Randau, L.,, M. Pearson, and, D. Söil. 2005. The complete set of RNA species in Nanoarchaeum equitans. FEBS Lett. 579 : 29452947.
47. Randau, L.,, R. Miinch,, M. J. Hohn,, D. Jahn, and, D. Söil. 2005. Nanoarchaeum equitans creates functional tRNAs from separate genes for their 5ʹ-and 3ʹ-halves. Nature 433 : 537541.
48. Ribas de Pouplana, L., and, P. Schimmel. 2001. Two classes of tRNA synthetases suggested by sterically compatible dockings on tRNA acceptor stem. Cell 104 : 191193.
49. Ruan, B., and, D. Söil. 2005. The bacterial YbaK protein is a Cys-tRNAPro and Cys-tRNACys deacylase. J. Biol. Chem. 280 : 2588725891.
50. Sauerwald, A.,, W. Zhu,, T. A. Major,, H. Roy,, S. Palioura,, D. Jahn,, W. B. Whitman,, J. R. Yates III,, M. Ibba, and, D. Soil. 2005. RNA-dependent cysteine biosynthesis in archaea. Science 307 : 19691972.
51. Schierling, K,, S. Rösch,, R. Rupprecht,, S. Schiffer, and, A. Marchfelder. 2002. tRNA 3-end maturation in archaea has eukaryotic features: the RNase Z from Haloferax volcanii. J. Mol. Biol. 316 : 895902.
52. Schiffer, S.,, S. Rösch, and, A. Marchfelder. 2003. Recombinant RNase Z does not recognize CCA as part of the tRNA and its cleavage efficiency is influenced by acceptor stem length. Biol. Chem. 384 : 333342.
53. Reference deleted.
54. She, Q.,, B. Shen, and, L. Chen. 2004. Archaeal integrases and mechanisms of gene capture. Biochem. Soc. Trans. 32 : 222226.
55. Schmitt, E.,, M. Panvert,, S. Blanquet, and, Y. Mechulam. 2005. Structural basis for tRNA-dependent amidotransferase function. Structure 13 : 14211433.
56. Soares, J. A.,, L. Zhang,, R. L. Pitsch,, N. M. Kleinholz,, R. B. Jones,, J. J. Wolff,, J. Amster,, K. B. Green-Church, and, J. A. Krzycki. 2005. The residue mass of L-pyrrolysine in three distinct methylamine methyltransferases. J. Biol. Chem. 280 : 3696236969.
57. Srinivasan, G.,, C. M. James, and, J. A. Krzycki. 2002. Pyrrolysine encoded by UAG in archaea: charging of a UAG-decoding specialized tRNA. Science 296 : 14591462.
58. Stathopoulos, C.,, W. Kim,, T. Li,, I. Anderson,, B. Deutsch,, S. Palioura,, W. Whitman, and, D. Soil. 2001. Cysteinyl-tRNA synthetase is not essential for viability of the archaeon Methanococcus maripaludis. Proc. Natl. Acad. Sci. USA 98 : 1429214297.
59. Tang, T. H.,, T. S. Rozhdestvensky,, B. C. d-Orval,, M. L. Bortoli., H. Huber,, B. Charpentier,, C. Branlant., J. P. Bachellerie,, J. Brosius, and, A. Hiittenhofer. 2002. RNomics in Archaea reveals a further link between splicing of archaeal introns and rRNA processing. Nucleic Acids Res. 30 : 921930.
60. Terada, T.,, O. Nureki,, R. Ishitani,, A. Ambrogelly,, M. Ibba,, D. Söil, and, S. Yokoyama. 2002. Functional convergence of two lysyl-tRNA synthetases with unrelated topologies. Nat. Struct. Biol. 9 : 257262.
61. Theobald-Dietrich, A.,, M. Frugier,, R. Giegé, and, J. Rudinger-Thirion. 2004. Atypical archaeal tRNA pyrrolysine transcript behaves towards EF-Tu as a typical elongator tRNA. Nucleic Acids Res. 32 : 10911096.
62. Theobald-Dietrich, A.,, R. Giegé, and, J. Rudinger-Thirion. 2005. Evidence for the existence in mRNAs of a hairpin element responsible for ribosome dependent pyrrolysine insertion into proteins. Biochimie 87 : 813817.
63. Thompson, L. D., and, C. J. Daniels. 1990. Recognition of exon-intron boundaries by the Halobacterium volcanii tRNA intron endonuclease. J. Biol. Chem. 265 : 1810418111.
64. Tocchini-Valentini, G. D.,, P. Fruscoloni, and, G. P. Tocchini-Valentini. 2005. Structure, function, and evolution of the tRNA endonucleases of Archaea: an example of subfunction-alization. Proc. Natl. Acad. Sci. USA 102 : 89338938.
65. Tumbula, D. L.,, H. D. Becker,, W.-Z. Chang, and, D. Söll. 2000. Domain-specific recruitment of amide amino acids for protein synthesis. Nature 407 : 106110.
66. Wang, L., and, P. G. Schultz. 2004. Expanding the genetic code. Angew. Chem. Int. Ed. Engl. 44 : 3466.
67. Watanabe, Y.,, S. Yokobori,, T. Inaba,, A. Yamagish., T. Oshima,, Y. Kawarabayasi,, H. Kikuchi, and, K. Kita. 2002. Introns in protein-coding genes in Archaea. FEBS Lett. 510: 2730.
68. >White, R. H. 2003. The biosynthesis of cysteine and homocysteine in Methanococcus jannaschii. Biochim. Biophys. Acta. 1624 : 4653.
69. Wilcox, M. 1969. Gamma-glutamyl phosphate attached to glutamine-specific tRNA. A precursor of glutaminyl-tRNA in Bacillus subtilis. Eur. J. Biochem. 11 : 40512.
70. Woese, C. R.,, G. J. Olsen,, M. Ibba, and, D. Söll. 2000. Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol. Mol. Biol. Rev. 64 : 202236.
71. Zhang, Y.,, P. V. Baranov,, J. F. Atkins, and, V. N. Gladyshev. 2005. Pyrrolysine and selenocysteine use dissimilar decoding strategies. J. Biol. Chem. 280 : 2074020751.
72. Zofallova, L.,, Y. Guo, and, R. Gupta,, R. 2000. Junction phosphate is derived from the precursor in the tRNA spliced by the archaeon Haloferax volcanii cell extract. RNA 6 : 10191030.

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