Home LiteratureArticle Details
PMID: 7642506 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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.

Journal of bacteriology ·Vol. 177 ·No. 16 ·1995-08-00 ·Pages 4779-91

Haase J, Lurz R, Grahn AM, Bamford DH, Lanka E

Abstract

DNA transfer by bacterial conjugation requires a mating pair formation (Mpf) system that specifies functions for establishing the physical contact between the donor and the recipient cell and for DNA transport across membranes. Plasmid RP4 (IncP alpha) contains two transfer regions designated Tra1 and Tra2, both of which contribute to Mpf. Twelve components are essential for Mpf, TraF of Tra1 and 11 Tra2 proteins, TrbB, -C, -D, -E, -F, -G, -H, -I, -J, -K, and -L. The phenotype of defined mutants in each of the Tra2 genes was determined. Each of the genes, except trbK, was found to be essential for RP4-specific plasmid transfer and for mobilization of the IncQ plasmid RSF1010. The latter process did not absolutely require trbF, but a severe reduction of the mobilization frequency occurred in its absence. Transfer proficiency of the mutants was restored by complementation with defined Tra2 segments containing single trb genes. Donor-specific phage propagation showed that traF and each of the genes encoded by Tra2 are involved. Phage PRD1, however, still adsorbed to the trbK mutant strain but not to any of the other mutant strains, suggesting the existence of a plasmid-encoded receptor complex. Strains containing the Tra2 plasmid in concert with traF were found to overexpress trb products as well as extracellular filaments visualized by electron microscopy. Each trb gene and traF are needed for the formation of the pilus-like structures. The trbK gene, which is required for PRD1 propagation and for pilus production but not for DNA transfer on solid media, encodes the RP4 entry-exclusion function. The components of the RP4 Mpf system are discussed in the context of related macromolecule export systems.

MeSH Terms
Amino Acid Sequence Bacterial Proteins/genetics,metabolism Base Sequence Biological Transport Cell Communication/genetics Coliphages/genetics Conjugation, Genetic/genetics DNA Mutational Analysis DNA, Bacterial/genetics,metabolism Escherichia coli/genetics,ultrastructure Fimbriae Proteins Genes, Bacterial/genetics Genetic Complementation Test Membrane Proteins/genetics Membranes/physiology Molecular Sequence Data Mutagenesis, Insertional Pili, Sex/genetics,ultrastructure Plasmids/genetics Sequence Analysis
Chemicals
Bacterial Proteins DNA, Bacterial Membrane Proteins TrbK protein, Plasmid RP4 Fimbriae Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Haase J
Max-Planck-Institut für Molekulare Genetik, Dahlem, Berlin, Germany.
Lurz R
Grahn A M
Bamford D H
Lanka E
References (79)
79 references, click to expand
  1. Analysis of the multimer resolution system encoded by the parCBA operon of broad-host-range plasmid RP4.
    Mol Microbiol. 1994 Apr;12(1):131-41 PMID: 8057833
  2. Sex pheromone plasmid pAD1-encoded surface exclusion protein of Enterococcus faecalis.
    Mol Gen Genet. 1992 May;233(1-2):161-8 PMID: 1603060
  3. Conjugative transfer functions of broad-host-range plasmid RK2 are coregulated with vegetative replication.
    Mol Microbiol. 1992 Apr;6(7):907-20 PMID: 1376390
  4. Mobilization of a Recombinant IncQ Plasmid between Bacteria on Agar and in Soil via Cotransfer or Retrotransfer.
    Appl Environ Microbiol. 1993 Jul;59(7):2257-63 PMID: 16348998
  5. The oriT region of the Agrobacterium tumefaciens Ti plasmid pTiC58 shares DNA sequence identity with the transfer origins of RSF1010 and RK2/RP4 and with T-region borders.
    J Bacteriol. 1992 Oct;174(19):6238-46 PMID: 1400174
  6. Initiation of Agrobacterium tumefaciens T-DNA processing. Purified proteins VirD1 and VirD2 catalyze site- and strand-specific cleavage of superhelical T-border DNA in vitro.
    J Biol Chem. 1995 Jan 20;270(3):1269-76 PMID: 7836390
  7. A single amino acid determinant of the membrane localization of lipoproteins in E. coli.
    Cell. 1988 May 6;53(3):423-32 PMID: 3284654
  8. Studies on transformation of Escherichia coli with plasmids.
    J Mol Biol. 1983 Jun 5;166(4):557-80 PMID: 6345791
  9. Entry exclusion determinant(s) of IncN plasmid pKM101.
    J Bacteriol. 1985 Jan;161(1):411-6 PMID: 2857163
  10. Covalent association of the traI gene product of plasmid RP4 with the 5'-terminal nucleotide at the relaxation nick site.
    J Biol Chem. 1990 Jun 25;265(18):10637-44 PMID: 2191955
  11. Regulation of transfer genes of promiscuous IncP alpha plasmid RK2: repression of Tra1 region transcription both by relaxosome proteins and by the Tra2 regulator TrbA.
    Microbiology. 1994 Nov;140 ( Pt 11):2981-90 PMID: 7812437
  12. The parDE operon of the broad-host-range plasmid RK2 specifies growth inhibition associated with plasmid loss.
    J Mol Biol. 1994 Mar 18;237(1):35-51 PMID: 8133518
  13. Construction and characterization of new cloning vehicles. VI. Plasmid pBR329, a new derivative of pBR328 lacking the 482-base-pair inverted duplication.
    Gene. 1982 Jan;17(1):79-89 PMID: 6281139
  14. Host range and properties of the Pseudomonas aeruginosa R factor R1822.
    J Bacteriol. 1973 Feb;113(2):772-80 PMID: 4632321
  15. Genetic interactions of broad host-range plasmid RK2: evidence for a complex replication regulon.
    Basic Life Sci. 1985;30:227-41 PMID: 2990411
  16. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector.
    Gene. 1986;48(1):119-31 PMID: 3549457
  17. Conjugal transfer system of plasmid RP4: analysis by transposon 7 insertion.
    J Bacteriol. 1978 Jan;133(1):43-52 PMID: 338595
  18. TraT lipoprotein, a plasmid-specified mediator of interactions between gram-negative bacteria and their environment.
    Microbiol Rev. 1990 Dec;54(4):331-41 PMID: 2087219
  19. Properties of an R factor from Pseudomonas aeruginosa.
    J Bacteriol. 1971 Dec;108(3):1244-9 PMID: 4945193
  20. Molecular characterization of an operon required for pertussis toxin secretion.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2970-4 PMID: 8464913
  21. Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid.
    J Biol Chem. 1988 Apr 25;263(12):5804-14 PMID: 3281947
  22. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes.
    Proc Natl Acad Sci U S A. 1985 Feb;82(4):1074-8 PMID: 3156376
  23. Entry exclusion of the IncN plasmid pKM101 is mediated by a single hydrophilic protein containing a lipid attachment motif.
    Plasmid. 1994 Mar;31(2):158-65 PMID: 8029323
  24. A genetic analysis of F sex factor cistrons needed for surface exclusion in Escherichia coli.
    J Mol Biol. 1980 Apr 25;138(4):779-95 PMID: 6997497
  25. Comparison of the lipid-containing bacteriophages PRD1, PR3, PR4, PR5 and L17.
    J Gen Virol. 1981 Dec;57(Pt 2):365-73 PMID: 7320707
  26. Expression of a cloned streptavidin gene in Escherichia coli.
    Proc Natl Acad Sci U S A. 1990 Jan;87(1):142-6 PMID: 2404273
  27. A complementation analysis of the restriction and modification of DNA in Escherichia coli.
    J Mol Biol. 1969 May 14;41(3):459-72 PMID: 4896022
  28. Common ancestry between IncN conjugal transfer genes and macromolecular export systems of plant and animal pathogens.
    Mol Microbiol. 1994 Nov;14(4):655-68 PMID: 7891554
  29. DNA processing reactions in bacterial conjugation.
    Annu Rev Biochem. 1995;64:141-69 PMID: 7574478
  30. Molecular and genetic analysis of a region of plasmid pCF10 containing positive control genes and structural genes encoding surface proteins involved in pheromone-inducible conjugation in Enterococcus faecalis.
    J Bacteriol. 1991 Dec;173(23):7650-64 PMID: 1938961
  31. The MURFI linker for multiple reading frame insertion of a sense or nonsense codon into DNA.
    Nucleic Acids Res. 1986 Mar 11;14(5):2139-55 PMID: 3008088
  32. Comparisons of the low-resolution structures of ornithine decarboxylase by electron microscopy and X-ray crystallography: the utility of methylamine tungstate stain and Butvar support film in the study of macromolecules by transmission electron microscopy.
    J Electron Microsc Tech. 1991 Jun;18(2):157-66 PMID: 1715911
  33. In vitro cleavage of double- and single-stranded DNA by plasmid RSF1010-encoded mobilization proteins.
    Nucleic Acids Res. 1992 Jan 11;20(1):41-8 PMID: 1738602
  34. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments.
    Gene. 1982 Oct;19(3):269-76 PMID: 6295880
  35. The virB operon of Agrobacterium tumefaciens pTiC58 encodes 11 open reading frames.
    Mol Gen Genet. 1990 Apr;221(2):256-66 PMID: 2370849
  36. The properties and host range of male-specific bacteriophages of Pseudomonas aeruginosa.
    J Gen Microbiol. 1974 Oct;84(2):332-42 PMID: 4217350
  37. Structure-independent DNA amplification by PCR using 7-deaza-2'-deoxyguanosine.
    Nucleic Acids Res. 1988 Oct 25;16(20):9869 PMID: 3186456
  38. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  39. KorB protein of promiscuous plasmid RP4 recognizes inverted sequence repetitions in regions essential for conjugative plasmid transfer.
    Nucleic Acids Res. 1992 Apr 25;20(8):1851-8 PMID: 1579485
  40. A common sequence motif, -E-G-Y-A-T-A-, identified within the primase domains of plasmid-encoded I- and P-type DNA primases and the alpha protein of the Escherichia coli satellite phage P4.
    J Biol Chem. 1992 Jun 25;267(18):13062-72 PMID: 1618804
  41. Complete nucleotide sequence of Birmingham IncP alpha plasmids. Compilation and comparative analysis.
    J Mol Biol. 1994 Jun 24;239(5):623-63 PMID: 8014987
  42. Promiscuous DNA transfer system of Agrobacterium tumefaciens: role of the virB operon in sex pilus assembly and synthesis.
    Mol Microbiol. 1994 Apr;12(1):17-22 PMID: 7914664
  43. Transposition of ampicillin resistance from RP4 to other replicons.
    Mol Gen Genet. 1974;132(1):31-40 PMID: 4609125
  44. 5'-3' exonucleases in phosphorothioate-based oligonucleotide-directed mutagenesis.
    Nucleic Acids Res. 1988 Feb 11;16(3):791-802 PMID: 2830593
  45. Two novel heat shock genes encoding proteins produced in response to heterologous protein expression in Escherichia coli.
    J Bacteriol. 1992 Nov;174(21):6938-47 PMID: 1356969
  46. 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):2493-500 PMID: 1556069
  47. Cell--cell interactions in conjugating Escherichia coli: role of traT protein in surface exclusion.
    Proc Natl Acad Sci U S A. 1977 Nov;74(11):5104-8 PMID: 337311
  48. 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):3089-95 PMID: 8387995
  49. Detection and subcellular localization of three Ptl proteins involved in the secretion of pertussis toxin from Bordetella pertussis.
    J Bacteriol. 1994 Sep;176(17):5350-6 PMID: 8071211
  50. Cloning of an exclusion-determining fragment of the IncI plasmid, R144.
    Plasmid. 1983 Jul;10(1):11-20 PMID: 6312474
  51. Specification of the conjugative pili and surface mating systems of Pseudomonas plasmids.
    J Gen Microbiol. 1983 Aug;129(8):2545-56 PMID: 6138393
  52. General organization of the conjugal transfer genes of the IncW plasmid R388 and interactions between R388 and IncN and IncP plasmids.
    J Bacteriol. 1990 Oct;172(10):5795-802 PMID: 2170327
  53. Essential motifs of relaxase (TraI) and TraG proteins involved in conjugative transfer of plasmid RP4.
    J Bacteriol. 1994 Jul;176(14):4285-95 PMID: 8021214
  54. The korF region of broad-host-range plasmid RK2 encodes two polypeptides with transcriptional repressor activity.
    J Bacteriol. 1991 Jan;173(2):826-33 PMID: 1987165
  55. Determination of pili by conjugative bacterial drug resistance plasmids of incompatibility groups B, C, H, J, K, M, V, and X.
    J Bacteriol. 1980 Feb;141(2):828-37 PMID: 6102552
  56. kil-kor regulon of promiscuous plasmid RK2: structure, products, and regulation of two operons that constitute the kilE locus.
    J Bacteriol. 1993 Aug;175(16):5078-90 PMID: 8349548
  57. The product of the F sex factor traT surface exclusion gene is a lipoprotein.
    J Biol Chem. 1984 May 10;259(9):5357-60 PMID: 6325433
  58. Localization and topology of VirB proteins of Agrobacterium tumefaciens.
    Plasmid. 1994 Sep;32(2):212-8 PMID: 7846145
  59. Site-specific deletions of chromosomally located DNA segments with the multimer resolution system of broad-host-range plasmid RP4.
    J Bacteriol. 1995 Jan;177(1):52-8 PMID: 7798149
  60. The protein sequence responsible for lipoprotein membrane localization in Escherichia coli exhibits remarkable specificity.
    J Biol Chem. 1991 Sep 5;266(25):16458-64 PMID: 1885579
  61. The essential virulence protein VirB8 localizes to the inner membrane of Agrobacterium tumefaciens.
    J Bacteriol. 1994 Mar;176(6):1711-7 PMID: 8132466
  62. Replication of mini RK2 plasmid in extracts of Escherichia coli requires plasmid-encoded protein TrfA and host-encoded proteins DnaA, B, G DNA gyrase and DNA polymerase III.
    J Mol Biol. 1988 Oct 20;203(4):927-38 PMID: 2850370
  63. 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):6666-73 PMID: 1400217
  64. Mobilization of the non-conjugative plasmid RSF1010: a genetic and DNA sequence analysis of the mobilization region.
    Mol Gen Genet. 1987 Jan;206(1):161-8 PMID: 3033438
  65. Characteristics of PRD1, a plasmid-dependent broad host range DNA bacteriophage.
    J Virol. 1974 Sep;14(3):689-99 PMID: 4211861
  66. Pedigrees of some mutant strains of Escherichia coli K-12.
    Bacteriol Rev. 1972 Dec;36(4):525-57 PMID: 4568763
  67. Identification and characterization of two entry exclusion genes of the promiscuous IncP plasmid R18.
    Mol Gen Genet. 1991 May;227(1):120-6 PMID: 1904533
  68. Active partitioning of bacterial plasmids.
    J Gen Microbiol. 1992 Jan;138(1):1-16 PMID: 1556544
  69. 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):20471-80 PMID: 1400366
  70. Characteristics and purification of PRR1, an RNA phage specific for the broad host range Pseudomonas R1822 drug resistance plasmid.
    J Virol. 1973 Dec;12(6):1560-7 PMID: 4128383
  71. The surface exclusion system of RP1: investigation of the roles of trbJ and trbK in the surface exclusion, transfer, and slow-growth phenotypes.
    Plasmid. 1994 Nov;32(3):254-61 PMID: 7899511
  72. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  73. In vitro assembly of relaxosomes at the transfer origin of plasmid RP4.
    Proc Natl Acad Sci U S A. 1990 Sep;87(17):6555-9 PMID: 2168553
  74. Adsorption of bacteriophages specific for Pseudomonas aeruginosa R factors RP1 and R1822.
    Biochem Biophys Res Commun. 1974 Apr 8;57(3):893-900 PMID: 4208062
  75. The mating pair formation system of plasmid RP4 defined by RSF1010 mobilization and donor-specific phage propagation.
    J Bacteriol. 1993 Oct;175(20):6415-25 PMID: 8407818
  76. Tn7 insertion mutations affecting the host range of the promiscuous IncP-1 plasmid R18.
    Plasmid. 1982 Sep;8(2):164-74 PMID: 6294704
  77. Common mechanisms in bacterial conjugation and Ti-mediated T-DNA transfer to plant cells.
    Cell. 1994 May 6;77(3):321-4 PMID: 8181052
  78. 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):287-94 PMID: 8405938
  79. Morphological and serological relationships of conjugative pili.
    Plasmid. 1980 Sep;4(2):155-69 PMID: 6152840
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1995-08-00
Pages
4779-91
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC177245
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com