Components of the RP4 conjugative transfer apparatus form an envelope structure bridging inner and outer membranes of donor cells: Implications for related macromolecule transport systems

Journal of Bacteriology

Volumn 182, Issue 6, 2000, Pages 1564-1574

  Grahn, A Marika ^a   Haase, Jana ^b   Bamford, Dennis H ^a   Lanka, Erich ^b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; GENE PRODUCT; NUCLEOPROTEIN; SINGLE STRANDED DNA;

ARTICLE; BACTERIAL MEMBRANE; BACTERIUM CONJUGATION; ENZYME ASSAY; ESCHERICHIA COLI; MACROMOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN TRANSPORT;

BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CELL FRACTIONATION; CELL MEMBRANE; CONJUGATION, GENETIC; DNA REPLICATION; ESCHERICHIA COLI; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; PERIPLASM; PLASMIDS; REPLICATION ORIGIN;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; PROKARYOTA;

EID: 0034050765     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.182.6.1564-1574.2000     Document Type: Article

References (71)

1. Alt-Mörbe, J., J. L. Stryker, C. Fuqua, P.-L. Li, S. K. Farrand, and S. C. Winans. 1996. The conjugal transfer system of Agrobacterium tumefaciens octopine-type Ti plasmid is closely related to the transfer system of an IncP plasmid and distantly related to Ti plasmid vir genes. J. Bacteriol. 178:4248-4257.
2. Balzer, D. 1993. Lokalisierung, Nukleotidsequenz und Genorganisation von IncP-Transferregionen. Freie Universität Berlin, Berlin, Germany.
3. Balzer, D., G. Ziegelin, W. Pansegrau, V. Kruft, and E. Lanka. 1992. KorB protein of promiscuous plasmid RP4 recognizes inverted sequence repetitions in regions essential for conjugative plasmid transfer. Nucleic Acids Res. 20:1851-C858.
4. Bamford, D. H., and L. Mindich. 1980. Electron microscopy of cells infected with nonsense mutants of bacteriophage phi 6. Virology 107:222-228.
5. Bates, S., A. M. Cashmore, and B. M. Wilkins. 1998. IncP plasmids are unusually effective in mediating conjugation of Escherichia coli and Saccharomyces cerevisiae: involvement of the Tra2 mating system. J. Bacteriol. 180:6538-6543.
6. Bayer, M. E. 1968. Areas of adhesion between wall and membrane of Escherichia coli. J. Gen. Microbiol. 53:395-404.
7. Beijersbergen, A., S. J. Smith, and P. J. J. Hooykaas. 1994. Localization and topology of VirB proteins of Agrobacterium tumefaciens. Plasmid 32:212-218.
8. Blobel, G. 1980. Intracellular protein topogenesis. Proc. Natl. Acad. Sci. USA 77:1496-1500.
9. Cabezón, E., J. I. Sastre, and F. de la Cruz. 1997. Genetic evidence of a coupling role for the TraG protein family in bacterial conjugation. Mol. Gen. Genet. 254:400-406.
10. Daugelavičius, R., J. K. H. Bamford, A. M. Grahn, E. Lanka, and D. H. Bamford. 1997. The IncP plasmid-encoded cell envelope-associated DNA transfer complex increases cell permeability. J. Bacteriol. 179:5195-5202.
11. de Maagd, R. A., and B. Lugtenberg. 1986. Fractionation of Rhizobium leguminosarum cells into outer membrane, cytoplasmic membrane, periplasmic, and cytoplasmic components. J. Bacteriol. 167:1083-1085.
12. Dürrenberger, M. B., W. Villiger, and T. Bächi. 1991. Conjugational junctions: morphology of specific contacts in conjugating Escherichia coli bacteria. J. Struct. Biol. 107:146-156.
13. Eisenbrandt, R., M. Kalkum, E.-M. Lai, R. Lurz, C. I. Kado, and E. Lanka. 1999. Conjugative pili of IncP plasmids and the Ti plasmid T pilus are composed of cyclic subunits. J. Biol. Chem. 274:22548-22555.
14. Farrand, S. K., I. Hwang, and D. M. Cook. 1996. The tra region of the nopaline-type Ti plasmid is a chimera with elements related to the transfer systems of RSF1010, RP4, and F. J. Bacteriol. 178:4233-4247.
15. Finberg, K. E., T. R. Muth, S. P. Young, J. B. Maken, S. M. Heitritter, A. N. Binns, and L. M. Banta. 1995. Interactions of VirB9, -10, and -11 with the membrane fraction of Agrobacterium tumefaciens: solubility studies provide evidence for tight associations. J. Bacteriol. 177:4881-4889.
16. Fürste, J. P., W. Pansegrau, R. Frank, H. Blöcker, P. Scholz, M. Bagdasarian, and E. Lanka. 1986. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene 43:119-131.
17. Fürste, J. P., W. Pansegrau, G. Ziegelin, M. Kröger, and E. Lanka. 1989. Conjugative transfer of promiscuous IncP plasmids: interaction of plasmid-encoded products with the transfer origin. Proc. Natl. Acad. Sci. USA 86: 1771-1775.
18. Gennity, J. M., and M. Inouye. 1991. The protein sequence responsible for lipoprotein membrane localization in Escherichia coli exhibits remarkable specificity. J. Biol. Chem. 266:16458-16454.
19. Grahn, A. M., J. Haase, E. Lanka, and D. H. Bamford. 1997. Assembly of a functional phage PRD1 receptor depends on 11 genes of the IncP plasmid mating pair formation complex. J. Bacteriol. 179:4733-4740.
20. Haase, J., M. Kalkum, and E. Lanka. 1996. TrbK, a small cytoplasmic membrane lipoprotein, functions in entry exclusion of the IncPα plasmid RP4. J. Bacteriol. 178:6720-6729.
21. Haase, J., and E. Lanka. 1997. A specific protease encoded by the conjugative DNA transfer systems of IncP and Ti plasmids is essential for pilus synthesis. J. Bacteriol. 179:5728-5735.
22. Haase, J., R. Lurz, A. M. Grahn, D. H. Bamford, and E. Lanka. 1995. Bacterial conjugation mediated by plasmid RP4: RSF1010 mobilization, donor-specific phage propagation, and pilus production require the same Tra2 core components of a proposed DNA transport complex. J. Bacteriol. 177:4779-4791.
23. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
24. Heinemann, J. A., and G. F. Sprague, Jr. 1989. Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast. Nature 340:205-209.
25. Hochuli, E., W. Bannwarth, H. Döbeli, R. Gentz, and D. Stüber. 1988. Genetic approach to facilitate purification of recombinant protein with a novel metal chelate adsorbent. Bio/Technology 6:1321-1325.
26. Hochuli, E., H. Döbeli, and A. Schacher. 1987. New metal chelate adsorbent selective for proteins and peptides containing neighbouring histidine residues. J. Chromatogr. 411:177-184.
27. Ishidate, K., E. S. Creeger, J. Zrike, S. Deb, B. Glauner, T. J. MacAlister, and L. I. Rothfield. 1986. Isolation of differentiated membrane domains from Escherichia coli and Salmonella typhimurium, including a fraction containing attachment sites between the inner and outer membranes and the murein skeleton of the cell envelope. J. Biol. Chem. 261:428-443.
28. Jackson, M. E., and J. M. Pratt. 1987. An 18 amino acid amphiphilic helix forms the membrane-anchoring domain of the Escherichia coli penicillin-binding protein 5. Mol. Microbiol. 1:23-28.
29. Johnson, D. J., and D. L. Burns. 1994. Detection and subcellular localization of three Ptl proteins involved in the secretion of pertussis toxin from Bordetella pertussis. J. Bacteriol. 176:5350-5356.
30. Kado, C. I. 1994. Promiscuous DNA transfer system of Agrobacterium tumefaciens: role of the virB operon in sex pilus assembly and synthesis. Mol. Microbiol. 12:17-22.
31. Kotilainen, M. M., A. M. Grahn, J. K. H. Bamford, and D. H. Bamford. 1993. Binding of an Escherichia coli double-stranded DNA virus PRD1 to a receptor coded by an IncP-type plasmid. J. Bacteriol. 175:3089-3095.
32. Kuldau, G. A., G. De Vos, J. Owen, G. McCaffrey, and P. Zambryski. 1990. The virB operon of Agrobacterium tumefaciens pTiC58 encodes 11 open reading frames. Mol. Gen. Genet. 221:256-266.
33. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
34. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
35. LaVallie, E. R., E. A. DiBlasio, S. Kovacic, K. L. Grant, P. F. Schendel, and J. M. McCoy. 1993. A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Bio/Technology 11:187-193.
36. Lessl, M., D. Balzer, R. Lurz, V. L. Waters, D. G. Guiney, and E. Lanka. 1992. Dissection of IncP conjugative plasmid transfer: definition of the transfer region Tra2 by mobilization of the Tra1 region in trans. J. Bacteriol. 174:2493-2500.
37. Lessl, M., D. Balzer, W. Pansegrau, and E. Lanka. 1992. Sequence similarities between the RP4 Tra2 and the Ti VirB region strongly support the conjugation model for T-DNA transfer. J. Biol. Chem. 267:20471-20480.
38. Lessl, M., D. Balzer, K. Weyrauch, and E. Lanka. 1993. The mating pair formation system of plasmid RP4 defined by RSF1010 mobilization and donor-specific phage propagation. J. Bacteriol. 175:6415-6425.
39. Lessl, M., and E. Lanka. 1994. Common mechanisms in bacterial conjugation and Ti-mediated T-DNA transfer to plant cells. Cell 77:321-324.
40. Miller, J. H. 1972. Experiments in molecular genetics, p. 431-433. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
41. Osborn, M. J., J. E. Gander, E. Parisi, and J. Carson. 1972. Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplsmic and outer membrane. J. Biol. Chem. 247: 3962-3972.
42. Pansegrau, W., and E. Lanka. 1996. Enzymology of DNA transfer by conjugative mechanisms. Prog. Nucleic Acid Res. Mol. Biol. 54:197-251.
43. Pansegrau, W., and E. Lanka. 1996. Mechanisms of initiation and termination reactions in conjugative DNA processing. Independence of tight substrate binding and catalytic activity of relaxase (TraI) of IncPα plasmid RP4. J. Biol. Chem. 271:13068-13076.
44. Pansegrau, W., E. Lanka, P. T. Barth, D. H. Figurski, D. G. Guiney, D. Haas, D. R. Helinski, H. Schwab, V. A. Stanisich, and C. M. Thomas. 1994. Complete nucleotide sequence of Birmingham IncPα plasmids. Compilation and comparative analysis. J. Mol. Biol. 239:623-663.
45. 2 synthase-1. Nature 367:243-249.
46. Pohlman, R. F., H. D. Genetti, and S. C. Winans. 1994. Common ancestry between IncN conjugal transfer genes and macromolecular export systems of plant and animal pathogens. Mol. Microbiol. 14:655-668.
47. Rost, B., R. Casadio, P. Fariselli, and C. Sander. 1995. Prediction of helical transmembrane segments at 95% accuracy. Protein Sci. 4:521-533.
48. Rost, B., P. Fariselli, and R. Casadio. 1996. Topology prediction for helical transmembrane proteins at 86% accuracy. Protein Sci. 5:1704-1718.
49. Rost, B., and C. Sander. 1993. Improved prediction of protein secondary structure by use of sequence profiles and neural networks. Proc. Natl. Acad. Sci. USA 90:7558-7562.
50. Rost, B., and C. Sander. 1993. Prediction of protein secondary structure at better than 70% accuracy. J. Mol. Biol. 232:584-599.
51. Rost, B., and C. Sander. 1994. Combining evolutionary information and neural networks to predict protein secondary structure. Proteins 19:55-72.
52. 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.
53. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
54. Schiffer, M., and A. B. Edmundson. 1967. Use of helical wheels to represent the structures of proteins and to identify segments with helical potential. Biophys. J. 7:121-135.
55. Schnaitman, C. A. 1970. Examination of the protein composition of the cell envelope of Escherichia coli by polyacrylamide gel electrophoresis. J. Bacteriol. 104:882-889.
56. Shirasu, K., and C. I. Kado. 1993. Membrane location of the Ti plasmid VirB proteins involved in the biosynthesis of a pilin-like conjugative structure on Agrobacterium tumefaciens. FEMS Microbiol. Lett. 111:287-294.
57. Shirasu, K., Z. Koukolikova-Nicola, B. Hohn, and C. I. Kado. 1994. An inner-membrane-associated virulence protein essential for T-DNA transfer from Agrobacterium tumefaciens to plants exhibits ATPase activity and similarities to conjugative transfer genes. Mol. Microbiol. 11:581-588.
58. Stachel, S. E., and P. C. Zambryski. 1986. Agrobacterium tumefaciens and the susceptible plant cell: a novel adaptation of extracellular recognition and DNA conjugation. Cell 47:155-157.
59. Thorsted, P. B., D. Macartney, P. Akhtar, A. S. Haines, N. Ali, P. Davidson, T. Stafford, M. Pocklington, W. Pansegrau, B. M. Wilkins, E. Lanka, and C. M. Thomas. 1998. Complete sequence of the IncPβ plasmid R751: implications for evolution and organisation of the IncP backbone. J. Mol. Biol. 282:969-990.
60. Thorstenson, Y. R., G. A. Kuldau, and P. C. Zambryski. 1993. Subcellular localization of seven VirB proteins of Agrobacterium tumefaciens: implications for the formation of a T-DNA transport structure. J. Bacteriol. 175:5233-5241.
61. Thorstenson, Y. R., and P. C. Zambryski. 1994. The essential virulence protein VirB8 localizes to the inner membrane of Agrobacterium tumefaciens. J. Bacteriol. 176:1711-1717.
62. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76:4350-4354.
63. Trieu-Cuot, P., C. Carlier, P. Martin, and P. Courvalin. 1987. Plasmid transfer by conjugation from Escherichia coli to gram-positive bacteria. FEMS Microbiol. Lett. 48:289-294.
64. von Heijne, G. 1986. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 14:4683-4690.
65. von Heijne, G. 1986. The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology. EMBO J. 5:3021-3027.
66. Ward, J. E., D. E. Akiyoshi, D. Regier, A. Datta, M. P. Gordon, and E. W. Nester. 1988. Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid. J. Biol. Chem. 263:5804-5814.
67. Ward, J. E., Jr., E. M. Dale, E. W. Nester, and A. N. Binns. 1990. Identification of a VirB10 protein aggregate in the inner membrane of Agrobacterium tumefaciens. J. Bacteriol. 172:5200-5210.
68. Waters, V. L., B. Strack, W. Pansegran, E. Lanka, and D. G. Guiney. 1992. Mutational analysis of essential IncPα plasmid transfer genes traF and traG and involvement of traF in phage sensitivity. J. Bacteriol. 174:6666-6673.
69. Weiss, A. A., F. D. Johnson, and D. L. Burns. 1993. Molecular characterization of an operon required for pertussis toxin secretion. Proc. Natl. Acad. Sci. USA 90:2970-2974.
70. Yamaguchi, K., F. Yu, and M. Inouye. 1988. A single amino acid determinant of the membrane localization of lipoproteins in E. coli. Cell 53:423-432.
71. Ziegelin, G. 1989. Konjugativer Transfer des IncP-Plasmids RP4: die Spezifitätsdeterminanten codieren oriT-Bindungsproteine. Freie Universität Berlin, Berlin, Germany.