A euryarchaeal Lysyl-tRNA synthetase: Resemblance to class I synthetases

Science

Volumn 278, Issue 5340, 1997, Pages 1119-1122

  Ibba, Michael ^a   Morgan, Susan ^b   Curnow, Alan W ^a   Pridmore, David R ^c   Vothknecht, Ute C ^a   Gardner, Warren ^d   Lin, Winston ^d   Woese, Carl R ^e   Söll, Dieter ^a  

^a YALE UNIVERSITY   (United States)

^b HAMILTON COLLEGE   (United States)

^c NESTLÉ RESEARCH CENTER   (Switzerland)

^d UNIVERSITY OF GEORGIA   (United States)

^e UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SYNTHETASE;

AMINO ACID SEQUENCE; AMINOACYLATION; ARTICLE; ENZYME ANALYSIS; GENOME; PRIORITY JOURNAL; SEQUENCE HOMOLOGY;

ACYLATION; AMINO ACID SEQUENCE; ANIMALS; BACTERIA; CLONING, MOLECULAR; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EURYARCHAEOTA; EVOLUTION, MOLECULAR; GENES, ARCHAEAL; HUMANS; KINETICS; LYSINE-TRNA LIGASE; METHANOCOCCUS; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, TRANSFER, AMINO ACYL; SEQUENCE ALIGNMENT; SULFOLOBUS;

EID: 0030707877     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.278.5340.1119     Document Type: Article

References (34)

1. J. Chen, A. Brevet, M. Lapadat-Taplosky, S. Blanquet, P. Plateau, J. Bacteriol. 176, 2699 (1994); F. Agou, S. Quevillon, P. Kerjan, M. T. Latreille, M. Mirande, Biochemistry 35, 15322 (1996); C. W. Sensen et al., Mol. Microbiol. 22, 175 (1996).
2. J. Chen, A. Brevet, M. Lapadat-Taplosky, S. Blanquet, P. Plateau, J. Bacteriol. 176, 2699 (1994); F. Agou, S. Quevillon, P. Kerjan, M. T. Latreille, M. Mirande, Biochemistry 35, 15322 (1996); C. W. Sensen et al., Mol. Microbiol. 22, 175 (1996).
3. J. Chen, A. Brevet, M. Lapadat-Taplosky, S. Blanquet, P. Plateau, J. Bacteriol. 176, 2699 (1994); F. Agou, S. Quevillon, P. Kerjan, M. T. Latreille, M. Mirande, Biochemistry 35, 15322 (1996); C. W. Sensen et al., Mol. Microbiol. 22, 175 (1996).
4. C. J. Bult et al., Science 273, 1058 (1996).
5. D. Smith et al., J. Bacteriol. in press.
6. A. W. Curnow, M. Ibba, D. Söll, Nature 382, 589 (1996).
7. M. Ibba, A. W. Curnow, D. Söll, Trends Biochem. Sci. 22, 39 (1997).
8. 14C-U]lysine (317 μCi/μmol; NEN Dupont, Boston, MA), and tRNA (1 mg/ml).
9. 14C were visualized by Phosphorlmager and internal standards by ninhydrin staining.
10. Frozen cells (20 g) were used to prepare an S160 extract as described (6), from which the major protein fraction was then separated by ammonium sulfate precipitation. This fraction was dialyzed and applied to a Q-Sepharose Fast Flow column that was then developed with an NaCl gradient (0 to 300 mM). LysRS-containing fractions were pooled, dialyzed, and then fractionated by anion-exchange chromatography with a Mono-Q column. Active fractions were again pooled and dialyzed, the pH was adjusted from 7.2 to 6, and the fractions were applied to a Mono-S cation-exchange column that was developed with an NaCl gradient (0 to 250 mM). The LysRS-containing samples were pooled and concentrated before they were applied to a Superose 12 gel filtration column [buffer A (pH 7.2)]. The LysRS fractions from this final step were judged to be pure by silver staining after SDS-PAGE. About 0.4 mg of LysRS was obtained by this procedure.
11. M value. Sampling and quantification were as described [K.-W. Hong et al., EMBO J. 15, 1983 (1996)].
12. W. Freist and D. H. Gauss, Biol. Chem. Hoppe-Seyler 376, 451 (1995).
13. M. Ibba and D. Söll, unpublished results. Significant lysylation represents at least 25% of the activity observed in the corresponding homologous system.
14. K. Tamura, H. Himeno, H. Ashahara, T. Hasegawa, M. Shimizu, Nucleic Acids Res. 20, 2335 (1992).
15. K. Watanabe et al., ibid. 22, 79 (1994); G. R. Björk, in tRNA: Structure, Biosynthesis, and Function, D. Söll and U. L. RajBhandary, Eds. (American Society for Microbiology, Washington, DC, 1995), pp. 165-205; S. Cusack, A. Yaremchuk, M. Tukalo, EMBO J. 15, 6321 (1996).
16. K. Watanabe et al., ibid. 22, 79 (1994); G. R. Björk, in tRNA: Structure, Biosynthesis, and Function, D. Söll and U. L. RajBhandary, Eds. (American Society for Microbiology, Washington, DC, 1995), pp. 165-205; S. Cusack, A. Yaremchuk, M. Tukalo, EMBO J. 15, 6321 (1996).
17. K. Watanabe et al., ibid. 22, 79 (1994); G. R. Björk, in tRNA: Structure, Biosynthesis, and Function, D. Söll and U. L. RajBhandary, Eds. (American Society for Microbiology, Washington, DC, 1995), pp. 165-205; S. Cusack, A. Yaremchuk, M. Tukalo, EMBO J. 15, 6321 (1996).
18. A. R. Kerlavage, The Institute for Genomic Research, Rockville, MD (http://www.tigr.org/tdb/mdb/mdb. html).
19. 6-LysRS, which was subsequently purified by nickel-affinity chromatography (QIAGEN) followed by gel filtration with a Superose 12 column (8).
20. R. Swanson, personal communication.
21. G. Eriani, M. Delarue, O. Poch, J. Gangloff, D. Moras, Nature 347, 203 (1990).
22. S. Cusack, Nature Struct. Biol. 2, 824 (1995).
23. S. Onesti, A. D. Miller, P. Brick, Structure 3, 163 (1995).
24. A phylogenetic tree was constructed by the maximum parsimony method [J. R. Brown and W. F. Doolittle, Proc. Natl. Acad. Sci. U.S.A. 92, 2441 (1995); G. M. Nagel and R. F. Doolittle, J. Mol. Evol. 40, 487 (1995)]. Amino acid sequences for the HIGH and KMSKS motifs and flanking residues were aligned with CLUSTAL W (26), and all insertions and deletions were then removed. A maximum-parsimony tree was derived with the programs SEQBOOT, PROTPARS, and CONSENSE from the PHYLIP 3.5c package [J. Felsenstein, Phylogeny Inference Package (Department of Genetics, Univ. of Washington, Seattle, WA, 1993)]. This procedure gave rise to a phylogenetic tree with low replicate frequencies for more than 50% of the nodes.
25. A phylogenetic tree was constructed by the maximum parsimony method [J. R. Brown and W. F. Doolittle, Proc. Natl. Acad. Sci. U.S.A. 92, 2441 (1995); G. M. Nagel and R. F. Doolittle, J. Mol. Evol. 40, 487 (1995)]. Amino acid sequences for the HIGH and KMSKS motifs and flanking residues were aligned with CLUSTAL W (26), and all insertions and deletions were then removed. A maximum-parsimony tree was derived with the programs SEQBOOT, PROTPARS, and CONSENSE from the PHYLIP 3.5c package [J. Felsenstein, Phylogeny Inference Package (Department of Genetics, Univ. of Washington, Seattle, WA, 1993)]. This procedure gave rise to a phylogenetic tree with low replicate frequencies for more than 50% of the nodes.
26. A phylogenetic tree was constructed by the maximum parsimony method [J. R. Brown and W. F. Doolittle, Proc. Natl. Acad. Sci. U.S.A. 92, 2441 (1995); G. M. Nagel and R. F. Doolittle, J. Mol. Evol. 40, 487 (1995)]. Amino acid sequences for the HIGH and KMSKS motifs and flanking residues were aligned with CLUSTAL W (26), and all insertions and deletions were then removed. A maximum-parsimony tree was derived with the programs SEQBOOT, PROTPARS, and CONSENSE from the PHYLIP 3.5c package [J. Felsenstein, Phylogeny Inference Package (Department of Genetics, Univ. of Washington, Seattle, WA, 1993)]. This procedure gave rise to a phylogenetic tree with low replicate frequencies for more than 50% of the nodes.
27. A. R. Mushegian and E. V. Koonin, Proc. Natl. Acad. Sci. U.S.A. 93, 10268 (1996).
28. R. A. Grayling, K. Sandman, J. N. Reeve, FEMS Microbiol. Rev. 18, 203 (1996); C. A. Ouzounis and N. C. Kyrpides, J. Mol. Evol. 42, 234 (1996).
29. R. A. Grayling, K. Sandman, J. N. Reeve, FEMS Microbiol. Rev. 18, 203 (1996); C. A. Ouzounis and N. C. Kyrpides, J. Mol. Evol. 42, 234 (1996).
30. A. Bergerat et al., Nature 386, 414 (1997).
31. K. Watanabe and S. Osawa, in tRNA: Structure, Biosynthesis, and Function, D. Söll and U. L. RajBhandary, Eds. (American Society for Microbiology, Washington, DC, 1995), pp. 225-250.
32. J. D. Thompson, D. G. Higgins, T. J. Gibson, Nucleic Acids Res. 22, 4673 (1994).
33. Abbreviations for the amino acid residues are as follows: A, Ala; C, Cys; D, Asp; E, Glu; F, Phe; G, Gly; H, His; I, Ile; K, Lys; L, Leu; M, Met; N, Asn; P, Pro; Q, Gln; R, Arg; S, Ser; T, Thr; V, Val; W, Trp; and Y, Tyr.
34. We thank D. Smith and Genome Therapeutics Corporation for access to M. thermoautotrophicum genome sequence data before publication; the W. M. Keck Foundation Biotechnology Resource Laboratory at Yale University for peptide sequencing and oligonucleotide synthesis; J. Deruère, M. Kitabatake, M. Kumar, M. Praetorius-Ibba, and S. Chaturvedi for advice on cloning strategies and providing materials; and A. Pfeifer and W. B. Whitman for advice and encouragement. Supported by a grant from Bristol-Myers Squibb (D.S.). The sequence of the M. maripaludis lysS gene has been deposited in GenBank (accession number AF009824).