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Identification of a novel gene, pilZ, essential for type 4 fimbrial biogenesis in Pseudomonas aeruginosa.

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  • 1. Centre for Molecular and Cellular Biology, University of Queensland, Brisbane, Australia.
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    • Alm RA 1
    (1 author)

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Journal of Bacteriology, 01 Jan 1996, 178(1):46-53
https://doi.org/10.1128/jb.178.1.46-53.1996 PMID: 8550441 PMCID: PMC177619

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Abstract 

The opportunistic pathogen Pseudomonas aeruginosa produces type 4 fimbriae which promote adhesion to epithelial cells and are associated with a form of surface translocation called twitching motility. We have used transposon mutagenesis to identify loci required for fimbrial assembly or function by screening for mutants that lack the spreading colony morphology characteristic of twitching motility. A subset of these mutants is resistant to fimbria-specific phage. One of these mutants (R270) was found to contain a transposon insertion in a new gene, termed pilZ, which is located on chromosomal SpeI fragment I at about 40 min on the P. aeruginosa map, a position remote from other loci involved in fimbrial biogenesis. pilZ appears to be linked to and possibly forms an operon with a gene, holB*, which is homologous to the gene encoding the delta' subunit of Escherichia coli DNA polymerase III. The product of the pilZ gene is a protein of 118 amino acids (predicted molecular weight, 12,895) which probably has a cytoplasmic location. PilZ appears to be a new class of protein which has not hitherto been represented in the sequence databases, and its function is unknown. Complementation studies indicate that pilZ is able to restore the expression of fimbriae on the surface of P. aeruginosa, as well as twitching motility and sensitivity to fimbria-specific phage when provided in trans to the R270 mutant.

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J Bacteriol. 1996 Jan; 178(1): 46–53.
PMCID: PMC177619
PMID: 8550441

Identification of a novel gene, pilZ, essential for type 4 fimbrial biogenesis in Pseudomonas aeruginosa.

R A Alm, A J Bodero, P D Free, and J S Mattick
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Abstract

The opportunistic pathogen Pseudomonas aeruginosa produces type 4 fimbriae which promote adhesion to epithelial cells and are associated with a form of surface translocation called twitching motility. We have used transposon mutagenesis to identify loci required for fimbrial assembly or function by screening for mutants that lack the spreading colony morphology characteristic of twitching motility. A subset of these mutants is resistant to fimbria-specific phage. One of these mutants (R270) was found to contain a transposon insertion in a new gene, termed pilZ, which is located on chromosomal SpeI fragment I at about 40 min on the P. aeruginosa map, a position remote from other loci involved in fimbrial biogenesis. pilZ appears to be linked to and possibly forms an operon with a gene, holB*, which is homologous to the gene encoding the delta' subunit of Escherichia coli DNA polymerase III. The product of the pilZ gene is a protein of 118 amino acids (predicted molecular weight, 12,895) which probably has a cytoplasmic location. PilZ appears to be a new class of protein which has not hitherto been represented in the sequence databases, and its function is unknown. Complementation studies indicate that pilZ is able to restore the expression of fimbriae on the surface of P. aeruginosa, as well as twitching motility and sensitivity to fimbria-specific phage when provided in trans to the R270 mutant.

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Selected References

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  • Alm RA, Dalrymple BP, Mattick JS. Sequencing and expression of the aroA gene from Dichelobacter nodosus. Gene. 1994 Jul 22;145(1):97–101. [Abstract] [Google Scholar]
  • Beard MK, Mattick JS, Moore LJ, Mott MR, Marrs CF, Egerton JR. Morphogenetic expression of Moraxella bovis fimbriae (pili) in Pseudomonas aeruginosa. J Bacteriol. 1990 May;172(5):2601–2607. [Europe PMC free article] [Abstract] [Google Scholar]
  • Begg KJ, Tomoyasu T, Donachie WD, Khattar M, Niki H, Yamanaka K, Hiraga S, Ogura T. Escherichia coli mutant Y16 is a double mutant carrying thermosensitive ftsH and ftsI mutations. J Bacteriol. 1992 Apr;174(7):2416–2417. [Europe PMC free article] [Abstract] [Google Scholar]
  • Bradley DE. Basic characterization of a Pseudomonas aeruginosa pilus-dependent bacteriophage with a long noncontractile tail. J Virol. 1973 Nov;12(5):1139–1148. [Europe PMC free article] [Abstract] [Google Scholar]
  • Brunschwig E, Darzins A. A two-component T7 system for the overexpression of genes in Pseudomonas aeruginosa. Gene. 1992 Feb 1;111(1):35–41. [Abstract] [Google Scholar]
  • Dalrymple B, Mattick JS. An analysis of the organization and evolution of type 4 fimbrial (MePhe) subunit proteins. J Mol Evol. 1987;25(3):261–269. [Abstract] [Google Scholar]
  • Darzins A. The pilG gene product, required for Pseudomonas aeruginosa pilus production and twitching motility, is homologous to the enteric, single-domain response regulator CheY. J Bacteriol. 1993 Sep;175(18):5934–5944. [Europe PMC free article] [Abstract] [Google Scholar]
  • Darzins A. Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus. Mol Microbiol. 1994 Jan;11(1):137–153. [Abstract] [Google Scholar]
  • Darzins A. The Pseudomonas aeruginosa pilK gene encodes a chemotactic methyltransferase (CheR) homologue that is translationally regulated. Mol Microbiol. 1995 Feb;15(4):703–717. [Abstract] [Google Scholar]
  • Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. [Europe PMC free article] [Abstract] [Google Scholar]
  • Elleman TC, Peterson JE. Expression of multiple types of N-methyl Phe pili in Pseudomonas aeruginosa. Mol Microbiol. 1987 Nov;1(3):377–380. [Abstract] [Google Scholar]
  • Hancock RE, Nikaido H. Outer membranes of gram-negative bacteria. XIX. Isolation from Pseudomonas aeruginosa PAO1 and use in reconstitution and definition of the permeability barrier. J Bacteriol. 1978 Oct;136(1):381–390. [Europe PMC free article] [Abstract] [Google Scholar]
  • Henrichsen J. Twitching motility. Annu Rev Microbiol. 1983;37:81–93. [Abstract] [Google Scholar]
  • Higgins DG, Sharp PM. Fast and sensitive multiple sequence alignments on a microcomputer. Comput Appl Biosci. 1989 Apr;5(2):151–153. [Abstract] [Google Scholar]
  • Hobbs M, Collie ES, Free PD, Livingston SP, Mattick JS. PilS and PilR, a two-component transcriptional regulatory system controlling expression of type 4 fimbriae in Pseudomonas aeruginosa. Mol Microbiol. 1993 Mar;7(5):669–682. [Abstract] [Google Scholar]
  • Hobbs M, Mattick JS. Common components in the assembly of type 4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes. Mol Microbiol. 1993 Oct;10(2):233–243. [Abstract] [Google Scholar]
  • Hoshino T, Kageyama M. Purification and properties of a binding protein for branched-chain amino acids in Pseudomonas aeruginosa. J Bacteriol. 1980 Mar;141(3):1055–1063. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hoyne PA, Haas R, Meyer TF, Davies JK, Elleman TC. Production of Neisseria gonorrhoeae pili (fimbriae) in Pseudomonas aeruginosa. J Bacteriol. 1992 Nov;174(22):7321–7327. [Europe PMC free article] [Abstract] [Google Scholar]
  • Koga T, Ishimoto K, Lory S. Genetic and functional characterization of the gene cluster specifying expression of Pseudomonas aeruginosa pili. Infect Immun. 1993 Apr;61(4):1371–1377. [Europe PMC free article] [Abstract] [Google Scholar]
  • Kyte J, Doolittle RF. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. [Abstract] [Google Scholar]
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. [Abstract] [Google Scholar]
  • Lauer P, Albertson NH, Koomey M. Conservation of genes encoding components of a type IV pilus assembly/two-step protein export pathway in Neisseria gonorrhoeae. Mol Microbiol. 1993 Apr;8(2):357–368. [Abstract] [Google Scholar]
  • Martin PR, Hobbs M, Free PD, Jeske Y, Mattick JS. Characterization of pilQ, a new gene required for the biogenesis of type 4 fimbriae in Pseudomonas aeruginosa. Mol Microbiol. 1993 Aug;9(4):857–868. [Abstract] [Google Scholar]
  • Mattick JS, Bills MM, Anderson BJ, Dalrymple B, Mott MR, Egerton JR. Morphogenetic expression of Bacteroides nodosus fimbriae in Pseudomonas aeruginosa. J Bacteriol. 1987 Jan;169(1):33–41. [Europe PMC free article] [Abstract] [Google Scholar]
  • McMichael JC. Bacterial differentiation within Moraxella bovis colonies growing at the interface of the agar medium with the Petri dish. J Gen Microbiol. 1992 Dec;138(12):2687–2695. [Abstract] [Google Scholar]
  • Normark S, Bergström S, Edlund T, Grundström T, Jaurin B, Lindberg FP, Olsson O. Overlapping genes. Annu Rev Genet. 1983;17:499–525. [Abstract] [Google Scholar]
  • Nunn DN, Lory S. Cleavage, methylation, and localization of the Pseudomonas aeruginosa export proteins XcpT, -U, -V, and -W. J Bacteriol. 1993 Jul;175(14):4375–4382. [Europe PMC free article] [Abstract] [Google Scholar]
  • Ottow JC. Ecology, physiology, and genetics of fimbriae and pili. Annu Rev Microbiol. 1975;29:79–108. [Abstract] [Google Scholar]
  • Paranchych W, Frost LS. The physiology and biochemistry of pili. Adv Microb Physiol. 1988;29:53–114. [Abstract] [Google Scholar]
  • Ratnaningsih E, Dharmsthiti S, Krishnapillai V, Morgan A, Sinclair M, Holloway BW. A combined physical and genetic map of Pseudomonas aeruginosa PAO. J Gen Microbiol. 1990 Dec;136(12):2351–2357. [Abstract] [Google Scholar]
  • Russell MA, Darzins A. The pilE gene product of Pseudomonas aeruginosa, required for pilus biogenesis, shares amino acid sequence identity with the N-termini of type 4 prepilin proteins. Mol Microbiol. 1994 Sep;13(6):973–985. [Abstract] [Google Scholar]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [Europe PMC free article] [Abstract] [Google Scholar]
  • Schweizer HP. Escherichia-Pseudomonas shuttle vectors derived from pUC18/19. Gene. 1991 Jan 2;97(1):109–121. [Abstract] [Google Scholar]
  • Shortridge VD, Pato ML, Vasil AI, Vasil ML. Physical mapping of virulence-associated genes in Pseudomonas aeruginosa by transverse alternating-field electrophoresis. Infect Immun. 1991 Oct;59(10):3596–3603. [Europe PMC free article] [Abstract] [Google Scholar]
  • Strom MS, Lory S. Structure-function and biogenesis of the type IV pili. Annu Rev Microbiol. 1993;47:565–596. [Abstract] [Google Scholar]
  • Strom MS, Nunn D, Lory S. Multiple roles of the pilus biogenesis protein pilD: involvement of pilD in excretion of enzymes from Pseudomonas aeruginosa. J Bacteriol. 1991 Feb;173(3):1175–1180. [Europe PMC free article] [Abstract] [Google Scholar]
  • Tomoyasu T, Yuki T, Morimura S, Mori H, Yamanaka K, Niki H, Hiraga S, Ogura T. The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATPases involved in membrane functions, cell cycle control, and gene expression. J Bacteriol. 1993 Mar;175(5):1344–1351. [Europe PMC free article] [Abstract] [Google Scholar]
  • Towbin H, Staehelin T, Gordon J. 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):4350–4354. [Europe PMC free article] [Abstract] [Google Scholar]
  • West SE, Iglewski BH. Codon usage in Pseudomonas aeruginosa. Nucleic Acids Res. 1988 Oct 11;16(19):9323–9335. [Europe PMC free article] [Abstract] [Google Scholar]
  • Whitchurch CB, Hobbs M, Livingston SP, Krishnapillai V, Mattick JS. Characterisation of a Pseudomonas aeruginosa twitching motility gene and evidence for a specialised protein export system widespread in eubacteria. Gene. 1991 May 15;101(1):33–44. [Abstract] [Google Scholar]
  • Whitchurch CB, Mattick JS. Characterization of a gene, pilU, required for twitching motility but not phage sensitivity in Pseudomonas aeruginosa. Mol Microbiol. 1994 Sep;13(6):1079–1091. [Abstract] [Google Scholar]
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