(βα)8-barrel proteins of tryptophan biosynthesis in the hyperthermophile Thermotoga maritima

EMBO Journal

Volumn 14, Issue 18, 1995, Pages 4395-4402

  Sterner, Reinhard ^a   Dahm, Anke ^a   Darimont, Beatrice ^b   Ivens, Andreas ^a   Liebl, Wolfgang ^c   Kirschner, Kasper ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Evolution of trp operon; Rare start codon; Salt bridges; Thermostability

Indexed keywords

BACTERIAL PROTEIN;

AMINO ACID COMPOSITION; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; CODON; ESCHERICHIA COLI; GENE CLUSTER; GENE SEQUENCE; MOLECULAR CLONING; NONHUMAN; OPERON; PRIORITY JOURNAL; THERMOPHILIC BACTERIUM; TRYPTOPHAN METABOLISM;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; THERMOTOGA MARITIMA;

EID: 0029114974     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1995.tb00118.x     Document Type: Article

References (45)

1. Achenbach-Richter,L., Gupta,R., Stetter,K.O. and Woese,C.R. (1987) Were the original eubacteria thermophiles? System. Appl. Microbiol., 9, 34-39.
2. Bachleitner,M., Ludwig,W., Stetter,K.O. and Schleifer,K.H. (1989) Nucleotide sequence of the gene coding for the elongation factor Tu from the extremely thermophilic eubacterium Thermotoga maritima. FEMS Microbiol. Lett., 57, 115-120.
3. Burggraf,S., Olsen,G.J., Stetter,K.O. and Woese,C.R. (1992) A phylogenetic analysis of Aquifex pyrophilus. System. Appl. Microbiol., 15, 352-356.
4. Cantatore,P., Roberti,M., Rainaldi,G., Gadaleta,N. and Saccone,C. (1989) The complete nucleotide sequence, gene organization, and genetic code of the mitochondrial genome of Paracentrotus lividus. J. Biol. Chem., 264, 10965-10975.
5. Cheng,Y.L., Kalman,L.V. and Kaiser,D. (1994) The dsg gene of Myxococcus xanthus encodes a protein similar to translation initiation factor IF3. J. Bacteriol., 176, 1427-1433.
6. Crawford,I.P. (1989) Evolution of a biosynthetic pathway: the tryptophan paradigm. Annu. Rev. Microbiol., 43, 567-600.
7. Darimont,B. (1994) Studies on catalysis, folding and evolution of indoleglycerol phosphate synthase, an eightfold βα-barrel protein involved in tryptophan biosynthesis. Ph.D. thesis, University of Basel, Switzerland.
8. Darimont,B. and Sterner,R. (1994) Sequence, assembly and evolution of a primordial ferredoxin from Thermotoga maritima. EMBO J., 13, 1772-1781.
9. D'Aubenton Carafa,Y., Brody,E. and Thermes,C. (1990) Prediction of rho-independent Escherichia coli transcription terminators. J. Mol. Biol., 216, 835-858.
10. Engel,A.M., Cejka,Z., Lupas,A., Lottspeich,F. and Baumeister,W. (1992) Isolation and cloning of Ompα, a coiled-coil protein spanning the periplasmic space of the ancestral eubacterium Thermotoga maritima. EMBO J., 11, 4369-4378.
11. Gold,L. (1988) Posttranscriptional regulation mechanisms in Escherichia coli. Annu. Rev. Biochem., 57, 199-233.
12. Gold,L. and Stormo,G. (1987) Translational initiation. In Neidhardt,F.C., Ingraham,J.L., Low,K.B., Magasanik,M., Schaechter,M. and Umbarger,H.E. (eds), Escherichia coli and Salomnella typhimurium: Cellular and Molecular Biology. American Society for Microbiology, Washington, DC, pp. 1302-1307.
13. Huber,R., Langworthy,T.A., König,H., Thomm,M., Woese,C.R., Sleytr,U.B. and Stetter,K.O. (1986) Thermotoga maritime sp. nov. represents a new genus of unique extremely thermophilic eubacterium growing up to 90°C. Arch. Microbiol., 144, 324-333.
14. 2 multienzyme complex from Salmonella typhimurium. J. Biol. Chem., 263, 17857-17871.
15. Jaenicke,R. (1991) Protein stability and molecular adaptation to extreme conditions. Eur. J. Biochem., 202, 715-728.
16. Jensen,R.A. (1992) An emerging outline of the evolutionary history of aromatic amino acid biosynthesis. In Mortlock,R.P (ed.). The Evolution of Metabolic Function. CRC Press, Boca Raton, FL, pp. 205-236.
17. Kelly,C.A., Nishiyama,M., Ohnishi,Y., Beppu,T. and Birktroft,JJ. (1993) Determinants of protein thermostability observed in the 1.9-Å crystal structure of malate dehydrogenase from the thermophilic bacterium Thermus flavus. Biochemistry, 32, 3913-3922.
18. Kim,C.W., Markiewicz,P., Lee,J.J., Schierle,C.F and Miller,J.H. (1993) Studies of the hyperthermophile Thermotoga maritima by random sequencing of cDNA and genomic libraries. J. Mol. Biol., 231, 960-981.
19. Korndörfer,I., Steipe,B., Huber,R., Tomschy,A. and Jaenicke,R. (1995) The crystal structure of holo-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga marilima at 2.5 Å resolution. J. Mol. Biol., 246, 511-521.
20. Kozak,M. (1983) Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol. Rev., 47, 1-45.
21. Laemmli,U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
22. Lam,W.L., Cohen,A., Tsouluhas,D. and Doolittle,W.F. (1990) Genes for tryptophan biosynthesis in the archaebacterium Haloferax volcanii. Proc. Natl Acad. Sci. USA, 87, 6614-6618.
23. Lam,W.L., Logan,S.M. and Doolittle,W.F. (1992) Genes for tryptophan biosynthesis in the halophilic archaebacterium Haloferax volcanii: the trpDFEG cluster. J. Bacteriol., 174, 1694-1697.
24. Liao,D. and Dennis,P.P. (1992) The organization and expression of essential transcription translation component genes in the extremely thermophilic eubacterium Thermotoga maritima. J. Biol. Chem., 267, 22787-22797.
25. Liebl,W., Gabelsberger,J. and Schleifer,K.-H. (1994) Comparative amino acid sequence analysis of Thermotoga maritima β-glucosidase (BglA) deduced from the nucleotide sequence of the gene indicates distant relationship between β-glucosidases of the BGA family and other families of β-1,4-glycosyl hydrolases. Mol. Gen. Genet., 242, 111-115.
26. Meile,L., Stettler,R., Banholzer,R., Kotik,M. and Leisinger,T. (1991) Tryptophan gene cluster of Methanobacterium thermoautorophicum Marburg: molecular cloning and nucleotide sequence of a putative rrpEGCFBAD operon. J. Bacteriol., 173, 5017-5023.
27. Niermann,T. and Kirschner,K. (1991) Improving the prediction of secondary structure of TIM-barrel enzymes. Protein Engng, 4, 359-370.
28. Ostendorp,R., Liebl,W., Schurig,H. and Jaenicke,R. (1993) The L-lactate dehydrogenase gene of the hyperthermophilic bacterium Thennotoga maritima cloned by complementation in Escherichia coli. Eur. J. Biochem., 216, 709-715.
29. Perutz,M.F. and Raidt,H. (1975) Stereochemical basis of heat stability in bacterial ferredoxins and in haemoglobin A2. Nature, 275, 256-259.
30. Priestle,J.R, Grütter,M.G., White,J.L., Vincent,M.G., Kania,M., Wilson,E., Jardetzky,T.S., Kirschner,K. and Jansonius,J.N. (1987) Three-dimensional structure of the bifunctional enzyme N-(5′-phosphoribosyl)anthranilate isomerase-indole-3-glycerol-phosphate synthase from Escherichia coli. Proc. Natl Acad. Sci. USA, 84, 5690-5694.
31. Reardon,D. and Farber,G.K. (1995) The structure and evolution of α/β barrel proteins. FASEB J., 9, 497-503.
32. Romero,A. and Garcia,P. (1991) Initiation of translation at AUC, AUA and AUU codons in Escherichia coli. EEMS Microbiol. Lett., 84, 325-330.
33. Sambrook,J., Fritsch,E.F, and Maniatis,E. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Sanangelantoni,A.M., Forlani,G., Ambroselli,F., Cammarano,P. and Tiboni,O. (1992) The glnA gene of the extremely thermophilic eubacterium Thermotoga maritima: cloning, primary structure, and expression in Escherichia coli. J. Gen. Microbiol., 138, 383-393.
35. Schurig,H., Beaucamp,N., Ostendorp,R., Jaenicke,R., Adler,E. and Knowles,J.R. (1995) Phosphoglycerate kinase and triosephosphate isomerase from the hyperthermophilic bacterium Thermotoga maritima form a covalent bifunctional enzyme complex. EMBO J., 14, 442-451.
36. Stetter,K.O., Fiala,G., Huber,G., Huber,R. and Segerer,A. (1990) Hyperthermophilic microorganisms, FEMS Microbiol. Rev., 75, 117-124.
37. Stewart,V. and Yanofsky,C. (1986) Role of leader peptide synthesis in tryptophanase operon expression in Escherichia coli K-12. J. Bacteriol., 167, 383-386.
38. Studier,F.W., Rosenberg,A.H., Dunn,J.J. and Dubendorff,J.W. (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol., 185, 60-89.
39. Tiboni,O., Sanangelantoni,A.M., Cammarano,P., Di Pasquale,G. and Sora,S. (1989) Expression in Escherichia coli of the tuf gene from the extremely thermophilic eubacterium Thermotoga maritima: purification of the Thermotoga elongation factor Tu by thermal denaturation of the mesophile host cell proteins. System. Appl. Microbiol., 12, 127-133.
40. Tomschy,A., Glockshuber,R. and Jaenicke,R. (1993) Functional expression of D-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic eubacterium Thermotoga maritima in Escherichia coli. Eur. J. Biochem., 214, 43-50.
41. Tutino,M.L., Scarano,G., Marino,G., Sannia,A. and Cubellis,M.V. (1993) Tryptophan biosynthesis genes trpEGC in the thermoacidophilic archaebacterium Sulfolobus soifataricus. J. Bactehol., 175, 299-302.
42. Wilmanns,M., Hyde,C.C., Davies,R.D., Kirschner,K. and Jansonius,J.N. (1991) Structural conservation in parallel β/α-barrel enzymes that catalyze three sequential reactions in the pathway of tryptophan biosynthesis. Biochemistry, 30, 9161-9169.
43. Wilmanns,M., Priestle,J.P. Niermann,T. and Jansonius,J.N. (1992) Three-dimensional structure of the bifunctional enzyme phosphoribosylanthranilate isomerase: indoleglycerolphosphate synthase from Escherichia coli refined at 2.0 A resolution. J. Mol. Biol., 223, 477-507.
44. Woese,C.R., Kandler,O. and Wheelis,M.L. (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA. 87, 4576-4579.
45. Yanofsky,C., Platt,T., Crawford,I.R. Nichols,B.P. Christie,G.E., Horowitz,H., VanCleemput,M. and Wu,A.M. (1981) The complete nucleotide sequence of the tryptophan operon of Escherichia coli. Nucleic Acids Res., 9, 6647-6668.