Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Aug;179(15):4733–4740. doi: 10.1128/jb.179.15.4733-4740.1997

Assembly of a functional phage PRD1 receptor depends on 11 genes of the IncP plasmid mating pair formation complex.

A M Grahn 1, J Haase 1, E Lanka 1, D H Bamford 1
PMCID: PMC179318  PMID: 9244259

Abstract

PRD1, a lipid-containing double-stranded DNA bacteriophage, uses the mating pair formation (Mpf) complex encoded by conjugative IncP plasmids as a receptor. Functions responsible for conjugative transfer of IncP plasmids are encoded by two distinct regions, Tra1 and Tra2. Ten Tra2 region gene products (TrbB to TrbL) and one from the Tra1 region (TraF) form the Mpf complex. We carried out a mutational analysis of the PRD1 receptor complex proteins by isolating spontaneous PRD1-resistant mutants. The mutations were distributed among the trb genes in the Tra2 region and accumulated predominantly in three genes, trbC, trbE, and trbL. Three of 307 phage-resistant mutants were weakly transfer proficient. Mutations causing a phage adsorption-deficient, transfer-positive phenotype were analyzed by sequencing.

Full Text

The Full Text of this article is available as a PDF (163.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Balzer D., Pansegrau W., Lanka E. Essential motifs of relaxase (TraI) and TraG proteins involved in conjugative transfer of plasmid RP4. J Bacteriol. 1994 Jul;176(14):4285–4295. doi: 10.1128/jb.176.14.4285-4295.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bamford D. H., Caldentey J., Bamford J. K. Bacteriophage PRD1: a broad host range DSDNA tectivirus with an internal membrane. Adv Virus Res. 1995;45:281–319. doi: 10.1016/s0065-3527(08)60064-0. [DOI] [PubMed] [Google Scholar]
  3. Bamford D. H., Mindich L. Characterization of the DNA-protein complex at the termini of the bacteriophage PRD1 genome. J Virol. 1984 May;50(2):309–315. doi: 10.1128/jvi.50.2.309-315.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bamford D., Mindich L. Structure of the lipid-containing bacteriophage PRD1: disruption of wild-type and nonsense mutant phage particles with guanidine hydrochloride. J Virol. 1982 Dec;44(3):1031–1038. doi: 10.1128/jvi.44.3.1031-1038.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bamford J. K., Bamford D. H. Capsomer proteins of bacteriophage PRD1, a bacterial virus with a membrane. Virology. 1990 Aug;177(2):445–451. doi: 10.1016/0042-6822(90)90508-o. [DOI] [PubMed] [Google Scholar]
  6. Boyer H. W., Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol. 1969 May 14;41(3):459–472. doi: 10.1016/0022-2836(69)90288-5. [DOI] [PubMed] [Google Scholar]
  7. Bradley D. E. Adsorption of bacteriophages specific for Pseudomonas aeruginosa R factors RP1 and R1822. Biochem Biophys Res Commun. 1974 Apr 8;57(3):893–900. doi: 10.1016/0006-291x(74)90630-5. [DOI] [PubMed] [Google Scholar]
  8. Bradley D. E. Adsorption of the R-specific bacteriophage PR4 to pili determined by a drug resistance plasmid of the W compatibility group. J Gen Microbiol. 1976 Jul;95(1):181–185. doi: 10.1099/00221287-95-1-181. [DOI] [PubMed] [Google Scholar]
  9. Bradley D. E. Morphological and serological relationships of conjugative pili. Plasmid. 1980 Sep;4(2):155–169. doi: 10.1016/0147-619x(80)90005-0. [DOI] [PubMed] [Google Scholar]
  10. Bradley D. E. Morphology of pili determined by the N incompatibility group plasmid N3 and interaction with bacteriophages PR4 and IKe. Plasmid. 1979 Oct;2(4):632–636. doi: 10.1016/0147-619x(79)90061-1. [DOI] [PubMed] [Google Scholar]
  11. Bradley D. E., Rutherford E. L. Basic characterization of a lipid-containing bacteriophage specific for plasmids of the P, N, and W compatibility groups. Can J Microbiol. 1975 Feb;21(2):152–163. doi: 10.1139/m75-023. [DOI] [PubMed] [Google Scholar]
  12. Butcher S. J., Bamford D. H., Fuller S. D. DNA packaging orders the membrane of bacteriophage PRD1. EMBO J. 1995 Dec 15;14(24):6078–6086. doi: 10.1002/j.1460-2075.1995.tb00298.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cabezón E., Lanka E., de la Cruz F. Requirements for mobilization of plasmids RSF1010 and ColE1 by the IncW plasmid R388: trwB and RP4 traG are interchangeable. J Bacteriol. 1994 Jul;176(14):4455–4458. doi: 10.1128/jb.176.14.4455-4458.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Caldentey J., Blanco L., Bamford D. H., Salas M. In vitro replication of bacteriophage PRD1 DNA. Characterization of the protein-primed initiation site. Nucleic Acids Res. 1993 Aug 11;21(16):3725–3730. doi: 10.1093/nar/21.16.3725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Davis T. N., Muller E. D., Cronan J. E., Jr The virion of the lipid-containing bacteriophage PR4. Virology. 1982 Jul 30;120(2):287–306. doi: 10.1016/0042-6822(82)90031-9. [DOI] [PubMed] [Google Scholar]
  16. Gennity J. M., Inouye M. The protein sequence responsible for lipoprotein membrane localization in Escherichia coli exhibits remarkable specificity. J Biol Chem. 1991 Sep 5;266(25):16458–16464. [PubMed] [Google Scholar]
  17. Haase J., Kalkum M., Lanka E. TrbK, a small cytoplasmic membrane lipoprotein, functions in entry exclusion of the IncP alpha plasmid RP4. J Bacteriol. 1996 Dec;178(23):6720–6729. doi: 10.1128/jb.178.23.6720-6729.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Haase J., Lurz R., Grahn A. M., Bamford D. H., Lanka E. 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. 1995 Aug;177(16):4779–4791. doi: 10.1128/jb.177.16.4779-4791.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kotilainen M. M., Grahn A. M., Bamford J. K., Bamford D. H. Binding of an Escherichia coli double-stranded DNA virus PRD1 to a receptor coded by an IncP-type plasmid. J Bacteriol. 1993 May;175(10):3089–3095. doi: 10.1128/jb.175.10.3089-3095.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lanka E., Wilkins B. M. DNA processing reactions in bacterial conjugation. Annu Rev Biochem. 1995;64:141–169. doi: 10.1146/annurev.bi.64.070195.001041. [DOI] [PubMed] [Google Scholar]
  21. Lessl M., Balzer D., Lurz R., Waters V. L., Guiney D. G., Lanka E. Dissection of IncP conjugative plasmid transfer: definition of the transfer region Tra2 by mobilization of the Tra1 region in trans. J Bacteriol. 1992 Apr;174(8):2493–2500. doi: 10.1128/jb.174.8.2493-2500.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lessl M., Balzer D., Pansegrau W., Lanka E. Sequence similarities between the RP4 Tra2 and the Ti VirB region strongly support the conjugation model for T-DNA transfer. J Biol Chem. 1992 Oct 5;267(28):20471–20480. [PubMed] [Google Scholar]
  23. Lessl M., Balzer D., Weyrauch K., Lanka E. The mating pair formation system of plasmid RP4 defined by RSF1010 mobilization and donor-specific phage propagation. J Bacteriol. 1993 Oct;175(20):6415–6425. doi: 10.1128/jb.175.20.6415-6425.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lundström K. H., Bamford D. H., Palva E. T., Lounatmaa K. Lipid-containing bacteriophage PR4: structure and life cycle. J Gen Virol. 1979 Jun;43(3):583–592. doi: 10.1099/0022-1317-43-3-583. [DOI] [PubMed] [Google Scholar]
  25. Lyra C., Savilahti H., Bamford D. H. High-frequency transfer of linear DNA containing 5'-covalently linked terminal proteins: electroporation of bacteriophage PRD1 genome into Escherichia coli. Mol Gen Genet. 1991 Aug;228(1-2):65–69. doi: 10.1007/BF00282449. [DOI] [PubMed] [Google Scholar]
  26. McConlogue L., Brow M. A., Innis M. A. Structure-independent DNA amplification by PCR using 7-deaza-2'-deoxyguanosine. Nucleic Acids Res. 1988 Oct 25;16(20):9869–9869. doi: 10.1093/nar/16.20.9869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mindich L., Bamford D., McGraw T., Mackenzie G. Assembly of bacteriophage PRD1: particle formation with wild-type and mutant viruses. J Virol. 1982 Dec;44(3):1021–1030. doi: 10.1128/jvi.44.3.1021-1030.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Olkkonen V. M., Bamford D. H. Quantitation of the adsorption and penetration stages of bacteriophage phi 6 infection. Virology. 1989 Jul;171(1):229–238. doi: 10.1016/0042-6822(89)90530-8. [DOI] [PubMed] [Google Scholar]
  29. Olsen R. H., Siak J. S., Gray R. H. Characteristics of PRD1, a plasmid-dependent broad host range DNA bacteriophage. J Virol. 1974 Sep;14(3):689–699. doi: 10.1128/jvi.14.3.689-699.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Pansegrau W., Lanka E., Barth P. T., Figurski D. H., Guiney D. G., Haas D., Helinski D. R., Schwab H., Stanisich V. A., Thomas C. M. Complete nucleotide sequence of Birmingham IncP alpha plasmids. Compilation and comparative analysis. J Mol Biol. 1994 Jun 24;239(5):623–663. doi: 10.1006/jmbi.1994.1404. [DOI] [PubMed] [Google Scholar]
  31. Pansegrau W., Lanka E. Enzymology of DNA transfer by conjugative mechanisms. Prog Nucleic Acid Res Mol Biol. 1996;54:197–251. doi: 10.1016/s0079-6603(08)60364-5. [DOI] [PubMed] [Google Scholar]
  32. Rost B., Casadio R., Fariselli P., Sander C. Transmembrane helices predicted at 95% accuracy. Protein Sci. 1995 Mar;4(3):521–533. doi: 10.1002/pro.5560040318. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Savilahti H., Bamford D. H. Linear DNA replication: inverted terminal repeats of five closely related Escherichia coli bacteriophages. Gene. 1986;49(2):199–205. doi: 10.1016/0378-1119(86)90280-5. [DOI] [PubMed] [Google Scholar]
  34. Savilahti H., Caldentey J., Lundström K., Syväoja J. E., Bamford D. H. Overexpression, purification, and characterization of Escherichia coli bacteriophage PRD1 DNA polymerase. In vitro synthesis of full-length PRD1 DNA with purified proteins. J Biol Chem. 1991 Oct 5;266(28):18737–18744. [PubMed] [Google Scholar]
  35. Shirasu K., Kado C. I. Membrane location of the Ti plasmid VirB proteins involved in the biosynthesis of a pilin-like conjugative structure on Agrobacterium tumefaciens. FEMS Microbiol Lett. 1993 Aug 1;111(2-3):287–294. doi: 10.1111/j.1574-6968.1993.tb06400.x. [DOI] [PubMed] [Google Scholar]
  36. Waters V. L., Strack B., Pansegrau W., Lanka E., Guiney D. G. Mutational analysis of essential IncP alpha plasmid transfer genes traF and traG and involvement of traF in phage sensitivity. J Bacteriol. 1992 Oct;174(20):6666–6673. doi: 10.1128/jb.174.20.6666-6673.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yamaguchi K., Yu F., Inouye M. A single amino acid determinant of the membrane localization of lipoproteins in E. coli. Cell. 1988 May 6;53(3):423–432. doi: 10.1016/0092-8674(88)90162-6. [DOI] [PubMed] [Google Scholar]
  38. Ziegelin G., Pansegrau W., Strack B., Balzer D., Kröger M., Kruft V., Lanka E. Nucleotide sequence and organization of genes flanking the transfer origin of promiscuous plasmid RP4. DNA Seq. 1991;1(5):303–327. doi: 10.3109/10425179109020786. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES