Chaperones specific for the membrane-bound [NiFe]-hydrogenase interact with the Tat signal peptide of the small subunit precursor in Ralstonia eutropha H16

Molecular Microbiology

Volumn 66, Issue 2, 2007, Pages 453-467

  Schubert, Torsten ^a   Lenz, Oliver ^a   Krause, Eberhard ^b   Volkmer, Rudolf ^c   Friedrich, Bärbel ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b LEIBNIZ INSTITUT FÜR MOLEKULARE PHARMAKOLOGIE   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; DIMER; HYDROGENASE; MEMBRANE ENZYME; SIGNAL PEPTIDE; TRANSACTIVATOR PROTEIN;

ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; CYTOPLASM; DIMERIZATION; ENZYME ACTIVITY; GENE DELETION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN ISOLATION; PROTEIN PROCESSING; WAUTERSIA EUTROPHA;

BACTERIAL PROTEINS; BASE SEQUENCE; CUPRIAVIDUS NECATOR; HYDROGENASE; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN SORTING SIGNALS;

CUPRIAVIDUS NECATOR;

EID: 34748882510     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.05933.x     Document Type: Article

References (59)

1. Berks, B.C., Sargent, F. Palmer, T. (2000) The Tat protein export pathway. Mol Microbiol 35 : 260 274.
2. Bernhard, M., Schwartz, E., Rietdorf, J. Friedrich, B. (1996) The Alcaligenes eutrophus membrane-bound hydrogenase gene locus encodes functions involved in maturation and electron transport coupling. J Bacteriol 178 : 4522 4529.
3. Bernhard, M., Benelli, B., Hochkoeppler, A., Zannoni, D. Friedrich, B. (1997) Functional and structural role of the cytochrome b subunit of the membrane-bound hydrogenase complex of Alcaligenes eutrophus H16. Eur J Biochem 248 : 179 186.
4. Bernhard, M., Friedrich, B. Siddiqui, R.A. (2000) Ralstonia eutropha TF93 is blocked in Tat-mediated protein export. J Bacteriol 182 : 581 588.
5. Böck, A., King, P.W., Blokesch, M. Posewitz, M.C. (2006) Maturation of hydrogenases. Adv Microbiol Physiol 51 : 1 71.
6. 2-sensing [NiFe] hydrogenase of Ralstonia eutropha. J Bacteriol 183 : 7087 7093.
7. +-reducing [NiFe]-hydrogenase from Ralstonia eutropha H16 consists of six subunits and can be specifically activated by NADPH. J Bacteriol 187 : 3122 3132.
8. Burgdorf, T., Lenz, O., Buhrke, T., van der Linden, E., Jones, A.K., Albracht, S.P. Friedrich, B. (2005b) [NiFe]-hydrogenases of Ralstonia eutropha H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation. J Mol Microbiol Biotechnol 10 : 181 196.
9. Chan, C.S., Howell, J.M., Workentine, M.L. Turner, R.J. (2006) Twin-arginine translocase may have a role in the chaperone function of NarJ from Escherichia coli. Biochem Biophys Res Commun 343 : 244 251.
10. Colbeau, A., Richaud, P., Toussaint, B., Caballero, J., Elster C., Delphin, C., et al. (1993) Organization of the genes necessary for hydrogenase expression in Rhodobacter capsulatus. Sequence analysis and identification of two hyp regulatory mutants. Mol Microbiol 8 : 15 29.
11. DeLisa, M.P., Tullman, D. Georgiou, G. (2003) Folding quality control in the export of proteins by the bacterial twin-arginine translocation pathway. Proc Natl Acad Sci USA 100 : 6115 6120.
12. Dernedde, J., Eitinger, T., Patenge, N. Friedrich, B. (1996) hyp gene products in Alcaligenes eutrophus are part of a hydrogenase-maturation system. Eur J Biochem 35 : 351 358.
13. Dubini, A. Sargent, F. (2003) Assembly of Tat-dependent [NiFe] hydrogenases: identification of precursor-binding accessory proteins. FEBS Lett 549 : 141 146.
14. Dubini, A., Pye, R., Jack, R., Palmer, T. Sargent, F. (2002) How bacteria get energy from hydrogen: a genetic analysis of periplasmic hydrogen oxidation in Escherichia coli. Int J Hydrogen Energy 27 : 1413 1420.
15. Fichtner, C., van Gastel, M. Lubitz, W. (2003) Wavelength dependence of the photo-induced conversion of the Ni-C to the Ni-L redox state in the [NiFe] hydrogenase of D. vulgaris Miyazaki F. Phys Chem Chem Phys 5 : 5507 5513.
16. Friedrich, C.G. (1982) Depression of hydrogenase during limitation of electron donors and derepression of ribulosebisphosphate carboxylase during carbon limitation of Alcaligenes eutrophus. J Bacteriol 149 : 203 210.
17. 2 sensor from Ralstonia eutropha. FEBS J 274 : 74 85.
18. Gross, R., Simon, J., Theis, F. Kröger, A. (1998) Two membrane anchors of Wolinella succinogenes hydrogenase and their function in fumarate and polysulfide respiration. Arch Microbiol 170 : 50 58.
19. Gross, R., Simon, J. Kröger, A. (1999) The role of the twin-arginine motif in the signal peptide encoded by the hydA gene of the hydrogenase from Wolinella succinogenes. Arch Microbiol 172 : 227 232.
20. Hatzixanthis, K., Clarke, T.A., Oubrie, A., Richardson, D.J., Turner, R.J. Sargent, F. (2005) Signal peptide-chaperone interactions on the twin-arginine protein transport pathway. Proc Natl Acad Sci USA 102 : 8460 8465.
21. Higuchi, Y., Yagi, T. Yasuoka, N. (1997) Unusual ligand structure in Ni-Fe active center and an additional Mg site in hydrogenase revealed by high resolution X-ray structure analysis. Structure 5 : 1671 1680.
22. Ilbert, M., Mejean, V., Giudici-Orticoni, M.T., Samama, J.P. Iobbi-Nivol, C. (2003) Involvement of a mate chaperone (TorD) in the maturation pathway of molybdoenzyme TorA. J Biol Chem 278 : 28787 28792.
23. Jack, R.L., Buchanan, G., Dubini, A., Hatzixanthis, K., Palmer, T. Sargent, F. (2004) Coordinating assembly and export of complex bacterial proteins. EMBO J 23 : 3962 3972.
24. Jones, A.K., Lenz, O., Strack, A., Buhrke, T. Friedrich, B. (2004) NiFe hydrogenase active site biosynthesis: identification of Hyp protein complexes in Ralstonia eutropha. Biochemistry 43 : 13467 13477.
25. 2 sensor of Ralstonia eutropha is a member of the subclass of regulatory [NiFe] hydrogenases. J Bacteriol 182 : 2716 2724.
26. Knüttel, K., Schneider, K., Erkens, A., Plass, W., Müller, A., Bill, E. Trautwein, A.X. (1994) Redox properties of the metal centres in the membrane-bound hydrogenase from Alcaligenes eutrophus CH34. Bull Pol Ac Sci Chem 42 : 495 511.
27. Kortlüke, C., Horstmann, K., Schwartz, E., Rohde, M., Binsack, R. Friedrich, B. (1992) A gene complex coding for the membrane-bound hydrogenase of Alcaligenes eutrophus H16. J Bacteriol 174 : 6277 6289.
28. Lambin, P. Fine, J.M. (1979) Molecular weight estimation of proteins by electrophoresis in linear polyacrylamide gradient gels in the absence of denaturing agents. Anal Biochem 98 : 160 168.
29. Lanciano, P., Vergnes, A., Grimaldi, S., Guigliarelli, B. Magalon, A. (2007) Biogenesis of a respiratory complex is orchestrated by a single accessory protein. J Biol Chem 282 : 17468 17474.
30. Leach, M.R. Zamble, D.B. (2007) Metallocenter assembly of the hydrogenase enzymes. Curr Opin Chem Biol 11 : 159 165.
31. Lenz, O., Schwartz, E., Dernedde, J., Eitinger, M. Friedrich, B. (1994) The Alcaligenes eutrophus H16 hoxX gene participates in hydrogenase regulation. J Bacteriol 176 : 4385 4393.
32. Lenz, O., Bernhard, M., Buhrke, T., Schwartz, E. Friedrich, B. (2002) The hydrogen-sensing apparatus in Ralstonia eutropha. J Mol Microbiol Biotechnol 4 : 255 262.
33. Lenz, O., Gleiche, A., Strack, A. Friedrich, B. (2005) Requirements for heterologous production of a complex metalloenzyme: the membrane-bound [NiFe] hydrogenase. J Bacteriol 187 : 6590 6595.
34. Manyani, H., Rey, L., Palacios, J.M., Imperial, J. Ruiz-Argüeso, T. (2005) Gene products of the hupGHIJ operon are involved in maturation of the iron-sulfur subunit of the [NiFe] hydrogenase from Rhizobium leguminosarum bv. viciae. J Bacteriol 187 : 7018 7026.
35. Menon, N.K., Robbins, J., Peck, H.D. Jr, Chatelus, C.Y., Choi, E.S. Przybyla, A.E. (1990) Cloning and sequencing of a putative Escherichia coli[NiFe] hydrogenase-1 operon containing six open reading frames. J Bacteriol 172 : 1969 1977.
36. Menon, N.K., Robbins, J., Wendt, J.C., Shanmugam, K.T. Przybyla, A.E. (1991) Mutational analysis and characterization of the Escherichia coli hya operon, which encodes [NiFe] hydrogenase 1. J Bacteriol 173 : 4851 4861.
37. Menon, A.L., Mortenson, L.E. Robson, R.L. (1992) Nucleotide sequences and genetic analysis of hydrogen oxidation (hox) genes in Azotobacter vinelandii. J Bacteriol 174 : 4549 4557.
38. Niviere, V., Wong, S.L. Voordouw, G. (1992) Site-directed mutagenesis of the hydrogenase signal peptide consensus box prevents export of a beta-lactamase fusion protein. J Gen Microbiol 183 : 2173 2183.
39. Oresnik, I.J., Ladner, C.L. Turner, R.J. (2001) Identification of a twin-arginine leader-binding protein. Mol Microbiol 40 : 323 331.
40. Palmer, T., Sargent, F. Berks, B.C. (2005) Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol 13 : 175 180.
41. Podzuweit, H.G., Schneider, K. Knüttel, H. (1987) Comparison of the membrane-bound hydrogenases from Alcaligenes eutrophus H16 and Alcaligenes eutrophus type strain. Biochim Biophys Acta 905 : 435 446.
42. Pohlmann, A., Fricke, W.F., Reinecke, F., Kusian, B., Liesegang, H., Cramm, R., et al. (2006) Genome sequence of the bioplastic-producing 'Knallgas' bacterium Ralstonia eutropha H16. Nat Biotechnol 24 : 1257 1262.
43. Probst, I. Schlegel, H.G. (1976) Respiratory components and oxidase activities in Alcaligenes eutrophus. Biochim Biophys Acta 440 : 412 428.
44. Ray, N., Oates, J., Turner, R.J. Robinson, C. (2003) DmsD is required for the biogenesis of DMSO reductase in Escherichia coli but not for the interaction of the DmsA signal peptide with the Tat apparatus. FEBS Lett 534 : 156 160.
45. 2-uptake gene cluster from Rhizobium leguminosarum bv. viciae containing a rubredoxin-like gene and four additional open reading frames. J Mol Biol 228 : 998 1002.
46. Rodrigue, A., Chanal, A., Beck, K., Müller, M. Wu, L.F. (1999) Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial tat pathway. J Biol Chem 274 : 13223 13228.
47. Sargent, F., Berks, B.C. Palmer, T. (2006) Pathfinders and trailblazers: a prokaryotic targeting system for transport of folded proteins. FEMS Microbiol Lett 254 : 198 207.
48. Schink, B. Schlegel, H.G. (1979) The membrane-bound hydrogenase of Alcaligenes eutrophus. I. Solubilization, purification, and biochemical properties. Biochim Biophys Acta 567 : 315 324.
49. Schneider, K. Schlegel, H.G. (1976) Purification and properties of soluble hydrogenase from Alcaligenes eutrophus H 16. Biochim Biophys Acta 452 : 66 80.
50. Schneider, K., Patil, D.S. Cammack, R. (1983) ESR properties of membrane-bound hydrogenases from aerobic hydrogen bacteria. Biochim Biophys Acta 748 : 353 361.
51. 2-metabolizing prokaryotes. In The Prokaryotes. Dworkin, M., Schleifer, K.H. Stackebrandt, E. (eds). New York : Springer, pp. 496 563.
52. 2-based lithoautotrophy and anaerobiosis. J Mol Biol 332 : 369 383.
53. Simon, R., Priefer, U. Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram-negative bacteria. Bio/Technology 1 : 784 791.
54. Towbin, H., Staehelin, T. Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76 : 4350 4354.
55. Turner, R.J., Papish, A.L. Sargent, F. (2004) Sequence analysis of bacterial redox enzyme maturation proteins (REMPs). Can J Microbiol 50 : 225 238.
56. Vignais, P.M., Billoud, B. Meyer, J. (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25 : 455 501.
57. Vincent, K.A., Cracknell, J.A., Lenz, O., Zebger, I., Friedrich, B. Armstrong, F. (2005) Electrocatalytic hydrogen oxidation by an enzyme at high carbon monoxide or hydrogen levels. Proc Natl Acad Sci USA 102 : 5033 5035.
58. Volbeda, A., Charon, M.H., Piras, C., Hatchikian, E.C., Frey, M. Fontecilla-Camps, J.C. (1995) Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373 : 580 587.
59. Yanisch-Perron, C., Vieira, J. Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33 : 103 119.