The Caulobacter crescentus paracrystalline S-layer protein is secreted by an ABC transporter (Type I) secretion apparatus

Journal of Bacteriology

Volumn 180, Issue 12, 1998, Pages 3062-3069

  Awram, Peter ^a   Smit, John ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ALKALINE PROTEINASE; METALLOPROTEINASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CAULOBACTER CRESCENTUS; CELL SURFACE; ERWINIA; MEMBRANE FUSION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; TRANSPOSON;

BACTERIA (MICROORGANISMS); CAULOBACTER CRESCENTUS; CAULOBACTER VIBRIOIDES; ERWINIA; ERWINIA CHRYSANTHEMI; NEGIBACTERIA; PROKARYOTA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 0031748720     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.180.12.3062-3069.1998     Document Type: Article

References (46)

1. Alley, M. R., S. L. Gomes, W. Alexander, and L. Shapiro. 1991. Genetic analysis of a temporally transcribed chemotaxis gene cluster in Caulobacter crescentus. Genetics 129:333-341.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Bik, E. M., A. E. Bunschoten, R. J. Willems, A. C. Chang, and F. R. Mooi. 1996. Genetic organization and functional analysis of the otn DNA essential for cell-wall polysaccharide synthesis in Vibrio cholerae O139. Mol. Microbiol. 20:799-811.
4. Binet, R., S. Letoffe, J. M, Ghigo, P. Delepelaire, and C. Wandersman. 1997. Protein secretion by Gram-negative bacterial ABC exporters - a review. Gene 192:7-11.
5. Bingle, W. H., K. D. Le, and J. Smit. 1996. The extreme N-terminus of the Caulobacter crescentus surface-layer protein directs export of passenger proteins from the cytoplasm but is not required for secretion of the native protein. Can. J. Microbiol. 42:672-684.
6. Bingle, W. H., J. F. Nomellini, and J. Smit. 1997. Cell-surface display of a Pseudomonas aeruginosa strain K pilin peptide within the paracrystalline S-layer of Caulobacter crescentus. Mol. Microbiol. 26:277-288.
7. Bingle, W. H., J. F. Nomellini, and J. Smit. 1997. Linker mutagenesis of the Caulobacter crescentus S-layer protein: toward a definition of an N-terminal anchoring region and a C-terminal secretion signal and the potential for heterologous protein secretion. J. Bacteriol. 179:601-611.
8. Bingle, W. H., and J. Smit. 1994. Alkaline phosphatase and a cellulase reporter protein are not exported from the cytoplasm when fused to large N-terminal portions of the Caulobacter crescentus surface (S)-layer protein. Can. J. Microbiol. 40:777-782.
9. Blaser, M. Personal communication.
10. Boot, H. J., and P. H. Pouwels. 1996. Expression, secretion and antigenic variation of bacterial S-layer proteins. Mol. Microbiol. 21:1117-1123.
11. Canter Cremers, H., H. P. Spaink, A. H. Wijfjes, E. Pees, C. A. Wiffelman, R. J. Okker, and B. J. Lugtenberg. 1989. Additional nodulation genes on the Sym plasmid of Rhizobium leguminosarum biovar viciae. Plant Mol. Biol. 13: 163-174.
12. Currie, H. L., J. Lightfoot, and J. S. Lam. 1995. Prevalence of gca, a gene involved in synthesis of A-band common antigen polysaccharide in Pseudomonas aeruginosa. Clin. Diag. Lab. Immunol. 2:554-562.
13. Delepelaire, P., and C. Wandersman. 1990. Protein secretion in gram-negative bacteria. The extracellular metalloprotease B from Erwinia chrysanthemi contains a C-terminal secretion signal analogous to that of Escherichia coli alpha-hemolysin. J. Biol. Chem. 265:17118-17125.
14. Dinh, T., I. T. Paulsen, and M. H. Saier, Jr. 1994. A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria. J. Bacteriol. 176:3825-3831.
15. Duong, F., A. Lazdunski, and M. Murgier. 1996. Protein secretion by heterologous bacterial ABC-transporters: the C-terminus secretion signal of the secreted protein confers high recognition specificity. Mol. Microbiol. 21: 459-470.
16. Dworkin, J., M. K. R. Tummuni, and M. J. Blaser. 1995. A lipopolysaccharide-binding domain of the Campylobacter fetus S-layer protein resides within the conserved N terminus of a family of silent and divergent homologs. J. Bacteriol. 177:1734-1741.
17. Edwards, P., and J. Smit. 1991. A transducing bacteriophage for Caulobacter crescentus uses the paracrystalline surface layer protein as a receptor. J. Bacteriol. 173:5568-5572.
18. Fellay, R., J. Frey, and H. Krisch. 1987. Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria. Gene 52:147-154.
19. Fisher, J. A., J. Smit, and N. Agabian. 1988. Transcriptional analysis of the major surface array gene of Caulobacter crescentus. J. Bacteriol. 170:4706-4713.
20. Ghigo, J. M., and C. Wandersman. 1992. Cloning, nucleotide sequence and characterization of the gene encoding the Erwinia chrysanthemi B374 PrtA metalloprotease: a third metalloprotease secreted via a C-terminal secretion signal. Mol. Gen. Genet. 236:135-144.
21. Gilchrist, A., J. A. Fisher, and J. Smit. 1992. Nucleotide sequence analysis of the gene encoding the Caulobacter crescentus paracrystalline surface layer protein. C. J. Microbiol. 38:193-202.
22. Gilchrist, A., and J. Smit. 1991. Transformation of freshwater and marine caulobacters by electroporation. J. Bacteriol. 173:921-925.
23. Guzzo, J., M. Murgier, A. Filloux, and A. Lazdunski. 1990. Cloning of the Pseudomonas aeruginosa alkaline protease gene and secretion of the protease into the medium by Escherichia coli. J. Bacteriol. 172:942-948.
24. Holton, T. A., and M. W. Graham. 1991. A simple and efficient method for direct cloning of PCR products using ddT-tailed vectors. Nucleic Acids Res. 19:1156.
25. Keen, N. T., S. Tamaki, D. Kobayashi, and D. Trollinger. 1988. Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70:191-197.
26. Kovach, M. E., R. W. Phillips, P. H. Elzer, R. M. Roop, and K. M. Peterson. 1994. pBBR1MCS: a broad-host-range cloning vector. BioTechniques 16: 800-802.
27. Koval, S. F., and S. H. Hynes. 1991. Effect of paracrystalline protein surface layers on predation by Bdellovibrio bacteriovorus. J. Bacteriol. 173:2244-2249.
28. Leeds, J. A., and R. A. Welch. 1996. RfaH enhances elongation of Escherichia coli hlyCABD mRNA. J. Bacteriol. 178:1850-1857.
29. Letoffe, S., P. Delepelaire, and C. Wandersman. 1990. Protease secretion by Erwinia chrysanthemi: the specific secretion functions are analogous to those of Escherichia coli alpha-haemolysin. EMBO J. 9:1375-1382.
30. Letoffe, S., and C. Wandersman. 1992. Secretion of CyaA-PrtB and HlyA-PrtB fusion proteins in Escherichia coli: involvement of the glycine-rich repeat domain of Erwinia chrysanthemi protease B. J. Bacteriol. 174:4920-4927.
31. Mead, D. A., E. Szczesna-Skorupa, and B. Kemper. 1986. Single-stranded DNA 'blue' T7 promoter plasmids: a versatile tandem promoter system for cloning and protein engineering. Protein Eng. 1:67-74.
32. Messner, P., and U. B. Sleytr. 1992. Crystalline bacterial cell-surface layers. Adv. Microb. Physiol. 33:213-275.
33. Nomellini, J. F., S. Kupcu, U. B. Sleytr, and J. Smit. 1997. Factors controlling in vitro recrystallization of the Caulobacter crescentus paracrystalline S-layer. J. Bacteriol. 179:6349-6354.
34. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
35. Ravenscroft, N., S. G. Walker, G. S. Dutton, and J. K. Smit. 1992. Identification, isolation, and structural studies of the outer membrane lipopolysaccharide of Caulobacter crescentus. J. Bacteriol. 174:7595-7605.
36. Salmond, G. P., and P. J. Reeves. 1993. Membrane traffic wardens and protein secretion in gram-negative bacteria. Trends Biochem. Sci. 18:7-12.
37. 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.
38. Simon, R., U. Priefer, and A. Puhier. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology 1:784-790.
39. Smit, J., and N. Agabian. 1984. Cloning of the major protein of the Caulobacter crescentus periodic surface layer: detection and characterization of the cloned peptide by protein expression assays. J. Bacteriol. 160:1137-1145.
40. Smit, J., H. Engelhardt, S. Volker, S. H. Smith, and W. Baumeister. 1992. The S-layer of Caulobacter crescentus: three-dimensional image reconstruction and structure analysis by electron microscopy. J. Bacteriol. 174:6527-6538.
41. Smit, J., D. A. Grano, R. M. Glaeser, and N. Agabian. 1981. Periodic surface array in Caulobacter crescentus: fine structure and chemical analysis. J. Bacteriol. 146:1135-1150.
42. Stroeher, U. H., L. E. Karageorgos, M. H. Brown, R. Morona, and P. A. Manning. 1995. A putative pathway for perosamine biosynthesis is the first function encoded within the rfb region of Vibrio cholerae Ol. Gene 166: 33-42.
43. Vieira, J., and J. Messing. 1982. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259-268.
44. Vuorio, R., T. Harkonen, M. Tolvanen, and M. Vaara. 1994. The novel hexapeptide motif found in the acyltransferases LpxA and LpxD of lipid A biosynthesis is conserved in various bacteria. FEBS Lett. 337:289-292.
45. Walker, S. G., D. N. Karunaratne, N. Ravenscroft, and J. Smit. 1994. Characterization of mutants of Caulobacter crescentus defective in surface attachment of the paracrystalline surface layer. J. Bacteriol. 176:6312-6323.
46. Walker, S. G., S. H. Smith, and J. Smit. 1992. Isolation and comparison of the paracrystalline surface layer proteins of freshwater caulobacters. J. Bacteriol. 174:1783-1792.