External loops at the C terminus of Erwinia chrysanthemi pectate lyase C are required for species-specific secretion through the out type II pathway

Journal of Bacteriology

Volumn 180, Issue 6, 1998, Pages 1431-1437

  Lindeberg, Magdalen ^a,c   Boyd, Carol M ^b   Keen, Noel T ^b   Collmer, Alan ^a  

^a Department of Population Medicine and Diagnostic Sciences   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HYBRID PROTEIN; PECTATE LYASE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL VIRULENCE; ERWINIA; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; SPECIES DIFFERENCE;

BACTERIA (MICROORGANISMS); ERWINIA; ERWINIA CAROTOVORA; ERWINIA CHRYSANTHEMI; ESCHERICHIA COLI; NEGIBACTERIA; PECTOBACTERIUM CAROTOVORUM;

EID: 0031891275     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.180.6.1431-1437.1998     Document Type: Article

References (56)

1. Ausubel, F. M., R. Brent, R. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1987. Current protocols in molecular biology. John Wiley & Sons. New York, N.Y.
2. Bally, M., G. Ball, A. Badere, and A. Lazdunski. 1991. Protein secretion in Pseudomonas aeruginosa: the xcpA gene encodes an integral inner membrane protein homologous to Klebsiella pneumoniae secretion function protein PulO. J. Bacteriol. 173:479-486.
3. Bally, M., A. Filloux, M. Akrim, G. Ball, A. Lazdunski, and J. Tommassen. 1992. Protein secretion in Pseudomonas aeruginosa: characterization of seven xcp genes and processing of secretory apparatus components by prepillin peptidase. Mol. Microbiol. 6:1121-1131.
4. Barras, F., F. Van Gijsegem, and A. K. Chatterjee. 1994. Extracellular enzymes and pathogenesis of soft-rot Erwinia. Annu. Rev. Phytopathol. 32:201-234.
5. Bortoli-German, I., E. Brun, B. Py, M. Chippaux, and F. Barras. 1994. Periplasmic disulphide bond formation is essential for cellulase secretion by the plant pathogen Erwinia chrysanthemi. Mol. Microbiol. 11:545-553.
6. 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. 92:248-254.
7. Chatterjee, A., Y. Liu, and A. K. Chatterjee. 1995. Nucleotide sequence of a pectate lyase structural gene, pell of Erwinia carotovora subsp. carotovora strain 71 and structural relationship of pell with other pel genes of Erwinia species. Mol. Plant-Microbe Interact. 8:92-95.
8. Collmer, A., J. L. Ried, and M. S. Mount. 1988. Assay methods for pectic enzymes. Methods Enzymol. 161:329-335.
9. d'Enfert, C., and A. P. Pugsley. 1987. A gene fusion approach to the study of pullulanase export and secretion in Escherichia coli. Mol. Microbiol. 1:159-168.
10. Dums, F., J. M. Dow, and M. J. Daniels. 1991. Structural characterization of protein secretion genes of the bacterial phytopathogen Xanthomonas campestris pathovar campestris: relatedness to secretion systems of other gram-negative bacteria. Mol. Gen. Genet. 229:357-364.
11. Fillloux, A., M. Bally, G. Ball, M. Akrim, J. Tommassen, and A. Lazdunski. 1990. Protein secretion in gram-negative bacteria: transport across the outer membrane involves common mechanisms in different bacteria. EMBO J. 9:4323-4329.
12. Hamood, A. N., J. C. Olson, T. S. Vincent, and B. H. Iglewski. 1989. Regions of toxin A involved in toxin A excretion in Pseudomonas aeruginosa. J. Bacteriol. 171:1817-1824.
13. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
14. He, S. Y., M. Lindeberg, A. K. Chatterjee, and A. Collmer. 1991. Cloned Erwinia chrysanthemi out genes enable Escherichia coli to selectively secrete a diverse family of heterologous proteins to its milieu. Proc. Natl. Acad. Sci. USA 88:1079-1083.
15. He, S. Y., C. Schoedel, A. K. Chatterjee, and A. Collmer. 1991. Extracellular secretion of pectate lyase by the Erwinia chrysanthemi Out pathway is dependent upon Sec-mediated export across the inner membrane. J. Bacteriol. 173:4310-4317.
16. Henrissat, B., S. E. Heffron, M. D. Yoder, S. Lietzke, and F. Jurnak. 1995. Functional implications of structure-based sequence alignment of proteins in the extracellular pectate lyase superfamily. Plant Physiol. 107:963-976.
17. Howard, S. P., J. Critch, and A. Bedi. 1993. Isolation and analysis of eight exe genes and their involvement in extracellular protein secretion and outer membrane assembly in Aeromonas hydrophila. J. Bacteriol. 175:6695-6703.
18. Hu, N.-T., M.-N. Hung, S-J. Chiou, F. Tang, D.-C. Chiang, H.-Y. Huang, and C.-Y. Wu. 1992. Cloning and characterization of a gene required for the secretion of extracellular enzymes across the outer membrane by Xanthomonas campestris pv. campestris. J. Bacteriol. 174:2679-2687.
19. Huang, J., M. Sukordhaman, and M. A. Schell. 1989. Excretion of the egl gene product of Pseudomonas solanacearum. J. Bacteriol. 171:3767-3774.
20. Jiang, B., and S. P. Howard. 1992. The Aeromonas hydrophila exeE gene, required both for protein secretion and normal outer membrane biogenesis, is a member of a general secretion pathway. Mol. Microbiol. 6:1351-1361.
21. 20a.Jurnak, F. Personal communication.
22. Kang, Y., J. Huang, M. Guozhang, L.-Y. He, and M. A. Schell. 1994. Dramatically reduced virulence of mutants of Pseudomonas solanacearum defective in export of extracellular proteins across the outer membrane. Mol. Plant-Microbe Interact. 7:370-377.
23. King, E., O., M. K. Ward, and D. E. Raney. 1954. Two simple media for the demonstration of pyocyanin and fluorescein. J. Lab. Med. 22:301-307.
24. Kita, N., C. M. Boyd, M. R. Garrett, F. Jurnak, and N. T. Keen. 1996. Differential effect of site-directed mutations in pelC on pectate lyase activity, plant tissue maceration, and elicitor activity. J. Biol. Chem. 271:26529-26535.
25. Kornacker, M. G., and A. P. Pugsley. 1989. Molecular characterization of pulA and its product, pullulanase, a secreted enzyme of Klebsiella pneumoniae UNF5023. Mol. Microbiol. 4:73-85.
26. Kornacker, M. G., and A. P. Pugsley. 1990. The normally periplasmic enzyme β-lactamase is specifically and efficiently translocated through the Escherichia coli outer membrane when it is fused to the cell-surface enzyme pullulanase. Mol. Microbiol. 4:1101-1109.
27. Kotoujansky, A. 1987. Molecular genetics of pathogenesis by soft-rot erwinias. Annu. Rev. Phytopathol. 25:405-430.
28. Lietzke, S. E., M. D. Yoder, N. T. Keen, and F. Jurnak. 1994. The three-dimensional structure of pectate lyase E, a plant virulence factor from Erwinia chrysanthemi. Plant Physiol. 106:849-862.
29. Lindeberg, M., and A. Collmer. 1992. Analysis of eight out genes in a cluster required for pectic enzyme secretion by Erwinia chrysanthemi: sequence comparison with secretion genes from other gram-negative bacteria. J. Bacteriol. 174:7385-7397.
30. Lindeberg, M., G. P. C. Salmond, and A. Collmer. 1996. Complementation of deletion mutations in a cloned functional cluster of Enwinia chrysanthemi out genes with Enwinia carotovora out homologs reveals OutC and OutD as candidate gatekeepers of species-specific secretion of proteins via the type II pathway. Mol. Microbiol. 20:175-190.
31. Lu, H.-M., and S. Lory. 1996. A specific targeting domain in mature exotoxin A is required for its extracellular secretion from Pseudomonas aeruginosa. EMBO J. 15:429-436.
32. McVay, C. S., and A. N. Hamood. 1995. Toxin A secretion in Pseudomonas aeruginosa: the role of the first 30 amino acids of the mature toxin. Mol. Gen. Genet. 249:515-525.
33. Mikaelian, I., and A. Sergeant. 1992. A general and fast method to generate multiple site directed mutations. Nucleic Acids Res. 20:376.
34. - mutants of Erwinia carotovora subsp. carotovora defective in enzyme export and of a DNA segment that complements out mutations in E. carotovora subsp. carotovora, E. carotovora subsp. atroseptica, and Erwinia chrysanthemi. J. Bacteriol. 172:2970-2978.
35. Overbye, L. J., M. Sandkvist, and M. Bagdasarian. 1993. Genes required for extracellular secretion of enterotoxin are clustered in Vibrio cholerae. Gene 132:101-106.
36. Palomaki, T., and H. T. Saarilathi. 1995. The extreme C-terminus is required for secretion of both the native polygalacturonase (PehA) and PehA-Bla hybrid proteins in Erwinia carotovora subsp. carotovora. Mol. Microbiol. 17:449-459.
37. Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85:2444-2448.
38. Peek, J. A., and R. K. Taylor. 1992. Characterization of periplasmic thiol: disulfide interchange protein required for the functional maturation of secreted virulence factors of Vibrio cholerae. Proc. Natl. Acad. Sci. USA 89: 6210-6214.
39. Pugsley, A. P. 1992. Translocation of a folded protein across the outer membrane in Escherichia coli. Proc. Natl. Acad. Sci. USA 89:12058-12062.
40. Pugsley, A. P. 1993. The complete general protein secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
41. Pugsley, A. P., C. d'Enfert, I. Reyss, and M. G. Kornacker. 1990. Genetics of extracellular protein secretion by gram-negative bacteria. Annu. Rev. Genet. 24:67-90.
42. Pugsley, A. P., O. Francetic, O. M. Possot, N. Sauvonnet, and K. R. Hardie. 1997. Recent progress and future directions in studies of the main terminal branch of the general secretory pathway in Gram-negative bacteria-a review. Gene 192:13-19.
43. Pugsley, A. P., I. Poquet, and M. G. Kornacker. 1991. Two distinct steps in pullulanase secretion by Escherichia coli K12. Mol. Microbiol. 5:865-873.
44. Py, B., M. Chippaux, and F. Barras. 1993. Mutagenesis of cellulase EGZ for studying the general protein secretory pathway. Mol. Microbiol. 7:785-793.
45. Py, B., G. P. C. Salmond, M. Chippaux, and F. Barras. 1991. Secretion of cellulases in Erwinia chrysanthemi and E. carotovora is species-specific. FEMS Microbiol. Lett. 79:315-322.
46. Reeves, P. J., D. Whitcombe, S. Wharam, M. Gibson, G. Allison, N. Bunce, R. Barallon, P. Douglas, V. Mulholland, S. Stevens, D. Walker, and G. P. C. Salmond. 1993. Molecular cloning and characterization of 13 out genes from Erwinia carotovora subspecies carotovora: genes encoding members of a general secretion pathway (GSP) widespread in gram-negative bacteria. Mol. Microbiol. 8:443-456.
47. Ried, J. L., and A. Collmer. 1985. An activity stain for the rapid characterization of pectic enzymes in isoelectric focusing and sodium dodecyl sulfate-polyacrylamide gels. Appl. Environ. Microbiol. 50:615-622.
48. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, N.Y.
49. Sauvonnet, N., and A. P. Pugsley. 1996. Identification of two regions of Klebsiella oxytoca pullulanase that together are capable of promoting beta-lactamase secretion by the general secretory pathway. Mol. Microbiol. 22: 1-7.
50. Schoepfer, R. 1993. The pRSET family of T7 promoter expression vectors for Escherichia coli. Gene 124:83-85.
51. Shevchik, V. E., G. Condemine, and J. Robert-Baudouy. 1994. Characterization of DsbC, a periplasmic protein of Erwinia chrysanthemi and Escherichia coli with disulfide isomerase activity. EMBO J. 13:1007-2012.
52. Shevchik, V. E., J. Robert-Baudouy, and G. Condemine. 1997. Specific interaction between OutD, an Erwinia chrysanthemi outer membrane protein of the general secretory pathway, and secreted proteins. EMBO J. 16:3007-3016.
53. Tamaki, S. J., S. Gold, M. Robeson, S. Manulis, and N. T. Keen. 1988. Structure and organization of the pel genes from Erwinia chrysanthemi EC16. J. Bacteriol. 170:3468-3478.
54. Wong, K. R., and J. T. Buckley. 1991. Site-directed mutagenesis of a single tryptophan near the middle of the channel-forming toxin aerolysin inhibits its transfer across the outer membrane of Aeromonas salmonicida. J. Biol. Chem. 266:14451-14456.
55. Yoder, M. D., N. T. Keen, and F. Jurnak. 1993. New domain motif: the structure of pectate lyase C, a secreted plant virulence factor. Science 260: 1503-1507.
56. Yu, J., H. Webb, and T. R. Hirst. 1992. A homolog of the Escherichia coli DsbA protein involved in disulphide bond formation is required for exotoxin biogenesis in Vibrio cholerae. Mol. Microbiol. 6:1949-1958.