Functional analysis of the twin-arginine translocation pathway in Corynebacterium glutamicum ATCC 13869

Applied and Environmental Microbiology

Volumn 72, Issue 11, 2006, Pages 7183-7192

  Kikuchi, Yoshimi ^a   Date, Masayo ^a   Itaya, Hiroshi ^a   Matsui, Kazuhiko ^a   Wu, Long Fei ^b  

^a AJINOMOTO CO INC   (Japan)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GENES; GENETIC ENGINEERING; MUTAGENESIS; PROTEINS; SUBSTRATES;

CORYNEBACTERIUM GLUTAMICUM TAT SYSTEM; GENOMES; GREEN FLUORESCENT PROTEIN (GFP); ISOMALTODEXTRANASE (IMD);

BACTERIA;

ARGININE; BACTERIAL PROTEIN; DEXTRANASE; GREEN FLUORESCENT PROTEIN; ISOMALTODEXTRANASE; ISOMALTOSE; PROTEIN TORA; SIGNAL PEPTIDE; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

BACTERIUM; BIOASSAY; GENETIC STRUCTURE; PROTEIN;

ARTHROBACTER GLOBIFORMIS; ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; CORYNEBACTERIUM GLUTAMICUM; ENTEROBACTERIACEAE; ESCHERICHIA COLI; GENE CONSTRUCT; GENE DELETION; GENE FUNCTION; GENE TRANSLOCATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FOLDING; PROTEIN MOTIF; SEQUENCE HOMOLOGY; TATA GENE; TATB GENE; TATC GENE; TATE GENE;

AMINO ACID SEQUENCE; ARTHROBACTER; BACTERIAL PROTEINS; CORYNEBACTERIUM GLUTAMICUM; DEXTRANASE; ESCHERICHIA COLI PROTEINS; GENE DELETION; GREEN FLUORESCENT PROTEINS; INDUSTRIAL MICROBIOLOGY; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; PROTEIN FOLDING; SEQUENCE ANALYSIS, DNA;

ARTHROBACTER GLOBIFORMIS; CORYNEBACTERIUM GLUTAMICUM; ENTEROBACTERIACEAE; ESCHERICHIA COLI; NEGIBACTERIA; POSIBACTERIA;

EID: 33750973650     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.01528-06     Document Type: Article

References (56)

1. Alami, M., I. Luke, S. Deitermann, G. Eisner, H. G. Koch, J. Brunner, and M. Müller. 2003. Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol. Cell 12:937-946.
2. Berks, B. C. 1996. A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22:393-404.
3. Berks, B. C., F. Sargent, and T. Palmer. 2000. The Tat protein export pathway. Mol. Microbiol. 35:260-274.
4. Blaudeck, N., P. Kreutzenbeck, M. Müller, G. A. Sprenger, and R. Freudl. 2005. Isolation and characterization of bifunctional Escherichia coli TatA mutant proteins that allow efficient tat-dependent protein translocation in the absence of TatB. J. Biol. Chem. 280:3426-3432.
5. Cerdeno-Tarraga, A. M., A. Efstratiou, L. G. Dover, M. T. Holden, M. Pallen, S. D. Bentley, G. S. Besra, C. Churcher, K. D. James, A. De Zoysa, T. Chillingworth, A. Cronin, L. Dowd, T. Feltwell, N. Hamlin, S. Holroyd, K. Jagels, S. Moule, M. A. Quail, E. Rabbinowitsch, K. M. Rutherford, N. R. Thomson, L. Unwin, S. Whitehead, B. G. Barrell, and J. Parkhill. 2003. The complete genome sequence and analysis of Corynebacterium diphtheriae NCTC13129. Nucleic Acids Res. 31:6516-6523.
6. Cline, K., R. Henry, C. Li, and J. Yuan. 1993. Multiple pathways for protein transport into or across the thylakoid membrane. EMBO J. 12:4105-4114.
7. Dabney-Smith, C., H. Mori, and K. Cline. 2006. Oligomers of Tha4 organize at the thylakoid Tat translocase during protein transport. J. Biol. Chem. 281:5476-5483.
8. Danese, P. N., and T. J. Silhavy. 1998. Targeting and assembly of periplasmic and outer-membrane proteins in Escherichia coli. Annu. Rev. Genet. 32:59-94.
9. Date, M., K. Yokoyama, Y. Umezawa, H. Matsui, and Y. Kikuchi. 2003. Production of native-type Streptoverticillium mobaraense transglutaminase in Corynebacterium glutamicum. Appl. Environ. Microbiol. 69:3011-3014.
10. Date, M., K. Yokoyama, Y. Umezawa, H. Matsui, and Y. Kikuchi. 2004. High level expression of Streptomyces mobaraensis transglutaminase in Corynebacterium glutamicum using a chimeric pro-region from Streptomyces cinnamoneus transglutaminase. J. Biotechnol. 110:219-226.
11. Date, M., K. Yokoyama, Y. Umezawa, H. Matsui, and Y. Kikuchi. 2006. Secretion of human epidermal growth factor by Corynebacterium glutamicum. Lett. Appl. Microbiol. 42:66-70.
12. De Keersmaeker, S., L. van Mellaert, E. Lammertyn, K. Vrancken, J. Anné, and N. Geukens. 2005. Functional analysis of TatA and TatB in Streptomyces lividans. Biochem. Biophys. Res. Commun. 335:973-982.
13. DeLisa, M. P., P. Samuelson, T. Palmer, and G. Georgiou. 2002. Genetic analysis of the twin-arginine translocator secretion pathway in bacteria. J. Biol. Chem. 277:29825-29831.
14. Di Cola, A., S. Bailey, and C. Robinson. 2005. The thylakoid delta pH/delta psi are not required for the initial stages of Tat-dependent protein transport in tobacco protoplasts. J. Biol. Chem. 280:41165-41170.
15. Feilmeier, B. J., G. Iseminger, D. Schroeder, H. Webber, and G. J. Phillips. 2000. Green fluorescent protein functions as a reporter for protein localization in Escherichia coli. J. Bacteriol. 182:4068-4076.
16. Fukui, K., J. Nakamura, and H. Kojima. December 2005. Succinic acid-producing bacterium and process for producing succinic acid. International Patent Cooperation Treaty patent WO2005/113744.
17. Gerard, F., and K. Cline. 2006. Efficient twin arginine translocation (Tat) pathway transport of a precursor protein covalently anchored to its initial cpTatC binding site. J. Biol. Chem. 281:6130-6135.
18. Gerlach, R., O. Pop, and J. P. Müller. 2004. Tat dependent export of E. coli phytase AppA by using the PhoD-specific transport system of Bacillus subtilis. J. Basic Microbiol. 44:351-359.
19. Gohlke, U., L. Pullan, C. A. McDevitt, I. Porcelli, E. de Leeuw, T. Palmer, H. R. Saibil, and B. C. Berks. 2005. The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. Proc. Natl. Acad. Sci. USA 102:10482-10486.
20. Gouffi, K., F. Gérard, C.-L. Santini, and L.-F. Wu. 2004. Dual topology of the Escherichia coli TatA protein. J. Biol. Chem. 279:11608-11615.
21. Hatada, Y., Y. Hidaka, Y. Nogi, K. Uchimura, K. Katayama, Z. Li, M. Akita, Y. Ohta, S. Goda, H. Ito, H. Matsui, S. Ito, and K. Horikoshi. 2004. Hyperproduction of an isomalto-dextranase of an Arthrobacter sp. by a proteases-deficient Bacillus subtilis: sequencing, properties, and crystallization of the recombinant enzyme. Appl. Microbiol. Biotechnol. 65:583-592.
22. Ikeda, M., and S. Nakagawa, S. 2003. The Corynebacterium glutamicum genome: features and impacts on biotechnological processes. Appl. Microbiol. Biotechnol. 62:99-109.
23. Iwai, A., H. Ito, T. Mizuno, H. Mori, H. Matsui, M. Honma, G. Okada, and S. Chiba. 1994. Molecular cloning and expression of an isomalto-dextranase gene from Arthrobacter globiformis T6. J. Bacteriol. 176:7730-7734.
24. Ize, B., F. Gérard, M. Zhang, A. Chanal, R. Voulhoux, T. Palmer, A. Filloux, and L.-F. Wu. 2002. In vivo dissection of the Tat translocation pathway in Escherichia coli. J. Mol. Biol. 317:327-335.
25. Ize, B., N. R. Stanley, G. Buchanan, and T. Palmer. 2003. Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol. Microbiol. 48:1183-1193.
26. Jack, R. L., F. Sargent, B. C. Berk, G. Sawers, and T. Palmer. 2001. Constitutive expression of Escherichia coli tat genes indicates an important role for the twin-arginine translocase during aerobic and anaerobic growth. J. Bacteriol. 183:1801-1804.
27. Jongbloed, J. D., U. Grieger, H. Antelmann, M. Hecker, R. Nijland, S. Bron, and J. M. van Dijl. 2004. Two minimal Tat translocases in Bacillus. Mol. Microbiol. 54:1319-1325.
28. Jongbloed, J. D., R. van der Ploeg, and J. M. van Dijl. 2006. Bifunctional TatA subunits in minimal Tat protein translocases. Trends Microbiol. 14:2-4.
29. Kalinowski, J., B. Bathe, D. Bartels, N. Bischoff, M. Bott, A. Burkovski, N. Dusch, L. Eggeling, B. J. Eikmanns, L. Gaigalat, A. Goesmann, M. Hartmann, K. Huthmacher, R. Kramer, B. Linke, A. C. McHardy, F. Meyer, B. Mockel, W. Pfefferle, A. Puhler, D. A. Rey, C. Ruckert, O. Rupp, H. Sahm, V. F. Wendisch, I. Wiegrabe, and A. Tauch. 2003. The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins. J. Biotechnol. 104:5-25.
30. Kesty, N. C., and M. J. Kuehn. 2004. Incorporation of heterologous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles. J. Biol. Chem. 279:2069-2076.
31. Kikuchi, Y., H. Kojima, T. Tanaka, Y. Takatsuka, and Y. Kamio. 1997. Characterization of a second lysine decarboxylase isolated from Escherichia coli. J. Bacteriol. 179:4486-4492.
32. Kikuchi, Y., M. Date, K. Yokoyama, Y. Umezawa, and H. Matsui. 2003. Secretion of active-form Streptoverticillium mobaraense transglutaminase by Corynebacterium glutamicum: processing of the pro-transglutaminase by a cosecreted subtilisin-like protease from Streptomyces albogriseolus. Appl. Environ. Microbiol. 69:358-366.
33. Krämer, R. 1994. Secretion of amino acids by bacteria: physiology and mechanism. FEMS Microbiol. Rev. 12:75-94.
34. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. Li, H., D. Faury, and R. Morosoli. 2006. Impact of amino acid changes in the signal peptide on the secretion of the Tat-dependent xylanase C from Streptomyces lividans. FEMS Microbiol. Lett. 255:268-274.
36. McDonough, J. A., K. E. Hacker, A. R. Flores, M. S. Pavelka, Jr., and M. Braunstein. 2005. The twin-arginine translocation pathway of Mycobacterium smegmatis is functional and required for the export of mycobacterial β-lactamases. J. Bacteriol. 187:7667-7679.
37. Müller, M., and R. B. Klosgen. 2005. The Tat pathway in bacteria and chloroplasts. Mol. Membr. Biol. 22:113-121.
38. Nishio, Y., Y. Nakamura, Y. Kawarabayasi, Y. Usuda, E. Kimura, S. Sugimoto, K. Matsui, A. Yamagishi, H. Kikuchi, K. Ikeo, and T. Gojobori. 2003. Comparative complete genome sequence analysis of the amino acid replacements responsible for the thermostability of Corynebacterium efficiens. Genome Res. 13:1572-1579.
39. Ormö, M., A. B. Cubitt, K. Kallio, L. A. Gross, R. Y. Tsien, and S. J. Remington. 1996. Crystal structure of the Aequorea victoria green fluorescent protein. Science 273:1392-1395.
40. Palmer, T., and B. C. Berks. 2003. Moving folded proteins across the bacterial cell membrane. Microbiology 149:547-556.
41. Posey, J. E., T. M. Shinnick, and F. D. Quinn. 2006. Characterization of the twin-arginine translocase secretion system of Mycobacterium smegmatis. J. Bacteriol. 188:1332-1340.
42. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
43. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
44. Santini, C.-L., A. Bernadac, M. Zhang, A. Chanal, B. Ize, C. Blanco, and L.-F. Wu. 2001. Translocation of jellyfish green fluorescent protein via the Tat system of Escherichia coli and change of its periplasmic localization in response to osmotic up-shock. J. Biol. Chem. 276:8159-8164.
45. Sargent, F., E. G. Bogsch, N. R. Stanley, M. Wexler, C. Robinson, B. C. Berks, and T. Palmer. 1998. Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J. 17:3640-3650.
46. Sargent, F., N. R. Stanley, B. C. Berks, and T. Palmer. 1999. Sec-independent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein. J. Biol. Chem. 274:36073-36082.
47. Schaerlaekens, K., M. Schierova, E. Lammertyn, N. Geukens, J. Anné, and L. van Mellaert. 2001. Twin-arginine translocation pathway in Streptomyces lividans. J. Bacteriol. 183:6727-6732.
48. Schaerlaekens, K., E. Lammertyn, N. Geukens, S. de Keersmaeker, J. Anné, and L. van Mellaert. 2004. Comparison of the Sec and Tat secretion pathways for heterologous protein production by Streptomyces lividans. J. Biotechnol. 112:279-288.
49. Spence, E., M. Sarcina, N. Ray, S. G. Moller, C. W. Mullineaux, and C. Robinson. 2003. Membrane-specific targeting of green fluorescent protein by the Tat pathway in the cyanobacterium Synechocystis PCC6803. Mol. Microbiol. 48:1481-1489.
50. Tauch, A., O. Kaiser, T. Hain, A. Goesmann, B. Weisshaar, A. Albersmeier, T. Bekel, N. Bischoff, I. Brune, T. Chakraborty, J. Kalinowski, F. Meyer, O. Rupp, S. Schneiker, P. Viehoever, and A. Puhler. 2005. Complete genome sequence and analysis of the multiresistant nosocomial pathogen Corynebacterium jeikeium K411, a lipid-requiring bacterium of the human skin flora. J. Bacteriol. 187:4671-4682.
51. Tinker, J. K., J. L. Erbe, and R. K. Holmes. 2005. Characterization of fluorescent chimeras of cholera toxin and Escherichia coli heat-labile enterotoxins produced by use of the twin arginine translocation system. Infect. Immun. 73:3627-3635.
52. Usuda, Y., H. Kawasaki, and T. Utagawa. 2001. Characterization of the cell surface protein gene of Corynebacterium ammoniagenes. Biochim. Biophys. Acta 1552:138-141.
53. Von Heijne, G. 1985. Signal sequences. The limits of variation. J. Mol. Biol. 184:99-105.
54. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
55. Yen, M. R., Y. H. Tseng, E. H. Nguyen, L.-F. Wu, and M. H. Saier, Jr. 2002. Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch. Microbiol. 177:441-450.
56. Yokoyama, K., N. Nakamura, K. Saguaro, and K. Kubota. 2000. Overproduction of microbial transglutaminase in Escherichia coli, in vitro refolding, and characterization of the refolded form. Biosci. Biotech. Biochem. 64:1263-1270.