Differential dependence of levansucrase and α-amylase secretion on SecA (Div) during the exponential phase of growth of Bacillus subtilis

Journal of Bacteriology

Volumn 181, Issue 6, 1999, Pages 1820-1826

  Leloup, Laurence ^a   Driessen, Arnold J M ^b   Freudl, Roland ^c   Chambert, Régis ^a   Petit Glatron, Marie Françoise ^a  

^a INSTITUT JACQUES MONOD   (France)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMYLASE; CARRIER PROTEIN; LEVANSUCRASE; PROTEIN; SIGNAL PEPTIDE; SODIUM AZIDE;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL GROWTH; BINDING AFFINITY; ENZYME REGULATION; ENZYME RELEASE; ENZYME SYNTHESIS; GROWTH CURVE; IMMUNOBLOTTING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; TEMPERATURE SENSITIVE MUTANT;

BACILLUS SUBTILIS;

EID: 0033064845     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.6.1820-1826.1999     Document Type: Article

References (52)

1. Berghöfer, J., I. Karnauchov, R. G. Hermann, and R. B. Klösgen. 1995. Isolation and characterization of a cDNA encoding the SecA protein from spinach chloroplasts. J. Biol. Chem. 270:18341-18346.
2. Blanco, J., J. J. Coque, and J. F. Martin. 1996. Characterization of the secA gene of Streptomyces lividans encoding a protein translocase which complements an Escherichia coli mutant defective in the ATPase activity of SecA. Gene 176:61-65.
3. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
4. h strain. J. Gen. Microbiol. 130:3143-3152.
5. Chambert, R., and M. F. Petit-Glatron. 1989. Study of the effect of organic solvents on the synthesis of levan and the hydrolysis of sucrose by Bacillus subtilis levansucrase. Carbohydr. Res. 191:117-123.
6. Cunningham, K., and W. Wickner. 1989. Specific recognition of the leader region of precursor proteins is required for the activation of translocation ATPase of Escherichia coli. Proc. Natl. Acad. Sci. USA 86:8630-8634.
7. den Blauwen, T., and A. J. M. Driessen. 1996. Sec-dependent preprotein translocation in bacteria. Arch. Microbiol. 165:1-8.
8. den Blauwen, T., P. Fekkes, J. G. de Wit, W. Kuiper, and A. J. M. Driessen. 1996. Domain interactions of the peripheral preprotein translocase subunit SecA. Biochemistry 35:11194-12004.
9. Driessen, A. J. M., P. Fekkes, and J. P. W. van der Wolk. 1998. The Sec system. Curr. Opin. Microbiol. 1:216-222.
10. Economou, A. 1998. Bacterial preprotein translocase: mechanism and conformational dynamics of a processive enzyme. Mol. Microbiol. 27:511-518.
11. Fortin, Y., P. Phoenix, and G. R. Drapeau. 1990. Mutations conferring resistance to azide in Escherichia coli occur primarily in the secA gene. J. Bacteriol. 172:6607-6610.
12. Haddaoui, E., L. Leloup, M. F. Petit-Glatron, and R. Chambert. 1997. Characterization of a stable intermediate trapped during reversible refolding of Bacillus subtilis α-amylase. Eur. J. Biochem. 249:505-509.
13. Hartl, F. U., S. Lecker, E. Schiebel, J. P. Hendrick, and W. Wickner. 1990. The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane. Cell 63:269-279.
14. Haward, S. R., J. A. Napier, and J. C. Gray. 1997. Chloroplast SecA functions as a membrane-associated component of the Sec-like protein translocase of pea chloroplasts. Eur. J. Biochem. 248:724-730.
15. Helde, R., B. Wieseler, E. Wachter, A. Neubüser, H. K. Hoffschulte, T. Hengelage, K.-L. Schimz, R. A. Stuart, and M. Müller. 1997. Comparative characterization of SecA from the α-subclass purple bacterium Rhodobacter capsulatus and Escherichia coli reveals differences in membrane and precursor specificity. J. Bacteriol. 179:4003-4012.
16. Kimura, E., M. Akita, S. Matsuyama, and S. Mizushima. 1991. Determination of a region in SecA that interacts with presecretory proteins in Escherichia coli. J. Biol. Chem. 266:6600-6606.
17. Klein, M., B. Hofmann, M. Klose, and R. Freudl. 1994. Isolation and characterization of a Bacillus subtilis secA mutant allele conferring resistance to sodium azide. FEMS Microbiol. Lett. 124:393-397.
18. Klein, M., J. P. Meens, and R. Freudl. 1995. Functional characterization of the Staphylococcus camosus SecA protein in Escherichia coli and Bacillus subtilis secA mutant strains. FEMS Microbiol. Lett. 131:271-277.
19. Klose, M., K. L. Schimz, J. P. W. van der Wolk, A. J. M. Driessen, and R. Freudl. 1993. Lysine 106 of the putative catalytic ATP-binding site of the Bacillus subtilis SecA protein is required for functional complementation of Escherichia coli secA mutants in vivo. J. Biol. Chem. 268:4504-4510.
20. Kraus, A., C. Hueck, D. Gärtner, and W. Hillen. 1994. Catabolite repression of the Bacillus subtilis xyl operon involves a cis element functional in the context of an unrelated sequence, and glucose exerts additional xylR-dependent repression. J. Bacteriol. 176:1738-1745.
21. Leloup, L., E. Haddaoui, R. Chambert, and M. F. Petit-Glatron. 1997. Characterization of the rate-limiting step of the secretion of Bacillus subtilis α-amylase overproduced during the exponential phase of growth. Microbiology 143:3295-3303.
22. Lepesant, J.-A., F. Kunst, M. Pascal, J. Kejzlarová-Lepesant, M. Steinmetz, and R. Dedonder. 1976. Specific and pleiotropic regulatory mechanisms in the sucrose system of Bacillus subtilis 168, p. 58-69. In D. Schlessinger (ed.), Microbiology - 1976. American Society for Microbiology, Washington, D.C.
23. Lill, R., K. Cunningham, L. A. Brundage, K. Ito, D. B. Oliver, and W. Wickner. 1989. SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase of Escherichia coli. EMBO J. 8:961-966.
24. Lill, R., W. Dowhan, and W. Wickner. 1990. The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins. Cell 60:271-280.
25. Lindner, C., J. Stülke, and M. Hecker. 1994. Regulation of xylanolytic enzymes in Bacillus subtilis. Microbiology 140:753-757.
26. McNicholas, P., T. Rajapandi, and D. Oliver. 1995. SecA proteins of Bacillus subtilis and Escherichia coli possess homologous amino-terminal ATP-binding domains regulating integration into the plasma membrane. J. Bacteriol. 177:7231-7237.
27. Meens, J. P., E. Frings, T. Klose, and R. Freudl. 1993. An outer membrane protein of Escherichia coli can be translocated across the cytoplasmic membrane of Bacillus subtilis. Mol. Microbiol. 9:847-855.
28. Mori, H., M. Araki, C. Hikita, M. Tagaya, and S. Mizushima. 1997. The hydrophobic region of signal peptides is involved in the interaction with membrane-bound SecA. Biochim. Biophys. Acta 1326:23-36.
29. Nakane, A., H. Takamatsu, A. Oguro, Y. Sadaie, K. Nakamura, and K. Yamane. 1995. Acquisition of azide-resistance by elevated SecA ATPase activity confers azide-resistance upon cell growth and protein translocation in Bacillus subtilis. Microbiology 141:113-121.
30. Oliver, D. B., and J. Beckwith. 1981. Escherichia coli pleiotropically defective in the export of secreted proteins. Cell 25:765-772.
31. Oliver, D. B., and J. Beckwith. 1982. Identification of a new gene (secA) and gene product involved in the secretion of envelope proteins in Escherichia coli. J. Bacteriol. 150:686-691.
32. Oliver, D. B., R. J. Cabelli, K. M. Dolan, and G. P. Jarosik. 1990. Azide-resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein translocation pathway. Proc. Natl. Acad. Sci. USA 87:8227-8231.
33. Oliver, D. B. 1993. SecA protein: autoregulated ATPase catalysing preprotein insertion and translocation across the Escherichia coli inner membrane. Mol. Microbiol. 7:159-165.
34. Petit-Glatron, M. F., F. Benyahia, and R. Chambert. 1987. Bacillus subtilis levansucrase: a possible two step mechanism. Eur. J. Biochem. 163:379-387.
35. Pöhling, S., W. Piepersberg, and U. F. Wehmeier. 1997. Protein secretion in Streptomyces griseus N2-3-11: characterization of the secA gene and its growth phase-dependent expression. FEMS Microbiol. Lett. 156:21-29.
36. Rajapandi, T., and D. B. Oliver. 1996. Integration of SecA protein into the Escherichia coli inner membrane is regulated by its amino-terminal ATP-binding domain. Mol. Microbiol. 20:43-51.
37. Rygus, T., and W. Hillen. 1991. Inducible high-level expression of heterologous genes in Bacillus megaterium using the regulatory elements of the xylose-utilisation operon. Appl. Microbiol. Biotechnol. 35:594-599.
38. Sadaie, Y., and T. Kada. 1983. Effect of septum-division mutations on sporulation and competent cell formation in Bacillus subtilis. Mol. Gen. Genet. 190:176-178.
39. Sadaie, Y., and T. Kada. 1985. Bacillus subtilis gene involved in cell division, sporulation, and exoenzyme secretion. J. Bacteriol. 163:648-653.
40. + gene of Bacillus subtilis to the Escherichia coli gene. Gene 98:101-105.
41. Schmidt, M. G., E. E. Rollo, J. Grodberg, and D. B. Oliver. 1988. Nucleotide sequence of the secA gene and secA(Ts) mutations preventing protein export in Escherichia coli. J. Bacteriol. 170:3404-3414.
42. Scotti, P., M. Praestegaard, R. Chambert, and M. F. Petit-Glatron. 1996. The targeting of Bacillus subtilis levansucrase in yeast is correlated to both the hydrophobicity of the signal peptide and the net charge of the N-terminus mature part. Yeast 12:953-963.
43. Scotti, P., R. Chambert, and M. F. Petit-Glatron. 1995. Kinetics of the unfolding-folding transition of Bacillus subtilis levansucrase precursor. FEBS Lett. 360:307-309.
44. Steinmetz, M., F. Kunst, and D. Dedonder. 1976. Mapping of mutations affecting synthesis of exocellular enzymes in Bacillus subtilis. Identity of the sacUh, amyB and pap mutations. Mol. Gen. Genet. 148:281-285.
45. Takamatsu, H., S.-I. Fuma, K. Nakamura, Y. Sadaie, A. Shinkai, S.-I. Matsuyama, S. Mizushima, and K. Yamane. 1992. In vivo and in vitro characterization of the secA gene product of Bacillus subtilis. J. Bacteriol. 174:4308-4316.
46. Takamatsu, H., A. Nakane, Y. Sadaie, K. Nakamura, and K. Yamane. 1994. The rapid degradation of mutant SecA protein in the Bacillus subtilis secA341 (ts) mutant causes a protein translocation defect in the cell. Biosci. Biotechnol. Biochem. 58:1845-1850.
47. Valentin, K. 1997. Phytogeny and expression of the secA gene from a chromophytic alga. Implications for the evolution of plastids and sec-dependent protein translocation. Curr. Genet. 32:300-307.
48. van der Wolk, J. P. W., M. Klose, E. Breukink, R. A. Demel, B. de Krujiff, R. Freudl, and A. J. M. Driessen. 1993. Characterization of a Bacillus subtilis SecA mutant protein deficient in translocation ATPase and release from the membrane. Mol. Microbiol. 8:31-42.
49. van der Wolk, J. P. W., M. Klose, J. G. de Wit, T. den Blaauwen, R. Freudl, and A. J. M. Driessen. 1995. Identification of the magnesium-binding domain of the high-affinity ATP-binding site of the Bacillus subtilis and Escherichia coli SecA protein. J. Biol. Chem. 270:18975-18982.
50. Varley, J. P., J. J. Moehrle, R. S. Manasse, D. S. Bendall, and C. J. Howe. 1995. Characterization of plastocyanin from cyanobacterium Phormidium laminosum: copper-inducible expression and SecA-dependent targeting in Escherichia coli. Plant Mol. Biol. 27:179-190.
51. Voelker, R., J. Mendel-Hartvig, and A. Barkan. 1997. Transposon-disruption of a maize nuclear gene, tha1, encoding a chloroplast SecA homologue: in vivo role of cp-SecA in thylakoid protein targeting. Genetics 145:467-478.
52. Yuan, J., R. Henry, M. McCaffery, and K. Cline. 1994. SecA homolog in protein transport within chloroplasts; evidence for endosymbiont-derived sorting. Science 266:796-801.