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PMID: 1355769 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, P.H.S.

Lesions in two Escherichia coli type 1 pilus genes alter pilus number and length without affecting receptor binding.

Journal of bacteriology ·Vol. 174 ·No. 18 ·1992-09-00 ·Pages 5923-35

Russell PW, Orndorff PE

Abstract

We describe the characterization of two genes, fimF and fimG (also called pilD), that encode two minor components of type 1 pili in Escherichia coli. Defined, in-frame deletion mutations were generated in vitro in each of these two genes. A double mutation that had deletions identical to both single lesions was also constructed. Examination of minicell transcription and translation products of parental and mutant plasmids revealed that, as predicted from the nucleotide sequence and previous reports, the fimF gene product was a protein of ca. 16 kDa and that the fimG gene product was a protein of ca. 14 kDa. Each of the constructions was introduced, via homologous recombination, into the E. coli chromosome. All three of the resulting mutants produced type 1 pili and exhibited hemagglutination of guinea pig erythrocytes. The latter property was also exhibited by partially purified pili isolated from each of the mutants. Electron microscopic examination revealed that the fimF mutant had markedly reduced numbers of pili per cell, whereas the fimG mutant had very long pili. The double mutant displayed the characteristics of both single mutants. However, pili in the double mutant were even longer than those seen in the fimG mutant, and the numbers of pili were even fewer than those displayed by the fimF mutant. All three mutants could be complemented in trans with a single-copy-number plasmid bearing the appropriate parental gene or genes to give near-normal parental piliation. On the basis of the phenotypes exhibited by the single and double mutants, we believe that the fimF gene product may aid in initiating pilus assembly and that the fimG product may act as an inhibitor of pilus polymerization. In contrast to previous studies, we found that neither gene product was required for type 1 pilus receptor binding.

Related Genes
MeSH Terms
Alleles Bacterial Adhesion/physiology Bacterial Proteins/biosynthesis,genetics Blotting, Southern DNA, Recombinant Endopeptidases Escherichia coli/genetics,ultrastructure Fimbriae, Bacterial/chemistry,physiology,ultrastructure Genetic Complementation Test Hemagglutination Tests Mutagenesis Polymerase Chain Reaction Receptors, Immunologic/physiology Transformation, Genetic
Chemicals
Bacterial Proteins DNA, Recombinant Receptors, Immunologic fimbriae receptor, type 1 Endopeptidases prepilin peptidase protein, Bacteria
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Russell P W
Department of Microbiology, Pathology, and Parasitology, North Carolina State University College of Veterinary Medicine, Raleigh 27606.
Orndorff P E
References (65)
65 references, click to expand
  1. Localization of the receptor-binding protein adhesin at the tip of the bacterial pilus.
    Nature. 1987 Jul 2-8;328(6125):84-7 PMID: 2885755
  2. Isolation and characterization of a receptor for type 1 fimbriae of Escherichia coli from guinea pig erythrocytes.
    J Biol Chem. 1988 Apr 15;263(11):5362-7 PMID: 2895767
  3. Investigation of minor components of Escherichia coli type 1 fimbriae: protein chemical and immunological aspects.
    Microb Pathog. 1988 Mar;4(3):231-8 PMID: 2904111
  4. Site-directed insertion and deletion mutagenesis with cloned fragments in Escherichia coli.
    J Bacteriol. 1985 Mar;161(3):1219-21 PMID: 2982787
  5. Metastable regulation of type 1 piliation in Escherichia coli and isolation and characterization of a phenotypically stable mutant.
    J Bacteriol. 1986 Oct;168(1):179-85 PMID: 3019997
  6. Two modes of control of pilA, the gene encoding type 1 pilin in Escherichia coli.
    J Bacteriol. 1985 Oct;164(1):321-30 PMID: 3930469
  7. Purification and properties of the recBC DNase of Escherichia coli K-12.
    J Biol Chem. 1972 Mar 25;247(6):1849-60 PMID: 4552016
  8. Molecular nature of two nonconjugative plasmids carrying drug resistance genes.
    J Bacteriol. 1974 Feb;117(2):619-30 PMID: 4590480
  9. Genetic recombination in Escherichia coli: the role of exonuclease I.
    Proc Natl Acad Sci U S A. 1971 Apr;68(4):824-7 PMID: 4927675
  10. K88ab gene of Escherichia coli encodes a fimbria-like protein distinct from the K88ab fimbrial adhesin.
    J Bacteriol. 1984 Aug;159(2):482-7 PMID: 6086572
  11. Binding specificity of piliated strains of Escherichia coli and Salmonella typhimurium to epithelial cells, saccharomyces cerevisiae cells, and erythrocytes.
    Infect Immun. 1981 May;32(2):796-804 PMID: 6114036
  12. Contribution of adhesion to bacterial persistence in the mouse urinary tract.
    Infect Immun. 1983 Apr;40(1):265-72 PMID: 6131870
  13. The role of pili and capsule in the pathogenesis of neonatal infection with Escherichia coli K1.
    J Infect Dis. 1983 Sep;148(3):395-405 PMID: 6137504
  14. Ultrastructural study of adhesion of enterotoxigenic Escherichia coli to erythrocytes and human intestinal epithelial cells.
    Infect Immun. 1984 May;44(2):519-27 PMID: 6143731
  15. Organization and expression of genes responsible for type 1 piliation in Escherichia coli.
    J Bacteriol. 1984 Aug;159(2):736-44 PMID: 6146599
  16. A system for shotgun DNA sequencing.
    Nucleic Acids Res. 1981 Jan 24;9(2):309-21 PMID: 6259625
  17. An amber replication mutant of F plasmid mapped in the minimal replication region.
    Mol Gen Genet. 1983;191(2):231-7 PMID: 6353162
  18. Construction and characterization of new cloning vehicles. III. Derivatives of plasmid pBR322 carrying unique Eco RI sites for selection of Eco RI generated recombinant DNA molecules.
    Gene. 1978 Oct;4(2):121-36 PMID: 363519
  19. Identification of the protein encoded by the transposable element Tn3 which is required for its transposition.
    Nature. 1979 Dec 20-27;282(5741):797-801 PMID: 390401
  20. Detection of specific sequences among DNA fragments separated by gel electrophoresis.
    J Mol Biol. 1975 Nov 5;98(3):503-17 PMID: 1195397
  21. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips.
    Nature. 1992 Mar 19;356(6366):252-5 PMID: 1348107
  22. A key role for type 1 pili in enterobacterial communicability.
    Mol Microbiol. 1992 Mar;6(6):697-701 PMID: 1349417
  23. Fragmentation of Escherichia coli type 1 fimbriae exposes cryptic D-mannose-binding sites.
    J Bacteriol. 1991 Jul;173(13):4195-202 PMID: 1676398
  24. Production of type 1 fimbriae by Escherichia coli HB101.
    Microb Pathog. 1991 Jun;10(6):481-6 PMID: 1686629
  25. The fimD gene required for cell surface localization of Escherichia coli type 1 fimbriae.
    Mol Gen Genet. 1990 Jan;220(2):334-8 PMID: 1970114
  26. Direct evidence that the FimH protein is the mannose-specific adhesin of Escherichia coli type 1 fimbriae.
    Infect Immun. 1990 Jun;58(6):1995-8 PMID: 1971261
  27. Effect of type 1 piliation on in vitro killing of Escherichia coli by mouse peritoneal macrophages.
    Infect Immun. 1990 Oct;58(10):3448-54 PMID: 1976116
  28. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid.
    J Bacteriol. 1978 Jun;134(3):1141-56 PMID: 149110
  29. A rapid alkaline extraction procedure for screening recombinant plasmid DNA.
    Nucleic Acids Res. 1979 Nov 24;7(6):1513-23 PMID: 388356
  30. Simple agarose gel electrophoretic method for the identification and characterization of plasmid deoxyribonucleic acid.
    J Bacteriol. 1976 Sep;127(3):1529-37 PMID: 821935
  31. Virulence of non-type 1-fimbriated and nonfimbriated nonflagellated Salmonella typhimurium mutants in murine typhoid fever.
    Infect Immun. 1992 Feb;60(2):491-6 PMID: 1346124
  32. Rapid site-specific DNA inversion in Escherichia coli mutants lacking the histonelike protein H-NS.
    J Bacteriol. 1991 Jul;173(13):4116-23 PMID: 1648076
  33. Type 1 fimbriae mutants of Escherichia coli K12: characterization of recognized afimbriate strains and construction of new fim deletion mutants.
    Mol Microbiol. 1991 Jun;5(6):1439-45 PMID: 1686292
  34. Impaired colonization by and full invasiveness of Escherichia coli K1 bearing a site-directed mutation in the type 1 pilin gene.
    Infect Immun. 1990 Jan;58(1):275-8 PMID: 1967169
  35. Genetic determinants coding for fimbriae and adhesins of extraintestinal Escherichia coli.
    Curr Top Microbiol Immunol. 1990;151:1-27 PMID: 1973366
  36. Isolation and characterization of mutants with lesions affecting pellicle formation and erythrocyte agglutination by type 1 piliated Escherichia coli.
    J Bacteriol. 1990 Nov;172(11):6411-8 PMID: 1977736
  37. Linkage map of Escherichia coli K-12, edition 8.
    Microbiol Rev. 1990 Jun;54(2):130-97 PMID: 2194094
  38. Nucleotide sequence of pilA, the gene encoding the structural component of type 1 pili in Escherichia coli.
    J Bacteriol. 1985 Apr;162(1):454-7 PMID: 2858471
  39. Role of type 1 pili and effects of phase variation on lower urinary tract infections produced by Escherichia coli.
    Infect Immun. 1985 Nov;50(2):370-7 PMID: 2865209
  40. Immunoelectron microscopic analysis of elongation of type 1 fimbriae in Escherichia coli.
    J Bacteriol. 1987 Jan;169(1):157-63 PMID: 2878917
  41. Phagolysosome formation by polymorphonuclear neutrophilic leukocytes after ingestion of Escherichia coli that express type 1 pili.
    J Infect Dis. 1987 Jul;156(1):229-33 PMID: 2885380
  42. Three fim genes required for the regulation of length and mediation of adhesion of Escherichia coli type 1 fimbriae.
    Mol Gen Genet. 1987 Jul;208(3):439-45 PMID: 2890081
  43. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  44. Lambdoid phages that simplify the recovery of in vitro recombinants.
    Mol Gen Genet. 1977 Jan 7;150(1):53-61 PMID: 319344
  45. Identification and characterization of E. coli type-1 pilus tip adhesion protein.
    Nature. 1988 Mar 17;332(6161):265-8 PMID: 2894612
  46. Identification of two ancillary subunits of Escherichia coli type 1 fimbriae by using antibodies against synthetic oligopeptides of fim gene products.
    J Bacteriol. 1987 Dec;169(12):5530-6 PMID: 2890622
  47. Hyperadhesive mutant of type 1-fimbriated Escherichia coli associated with formation of FimH organelles (fimbriosomes).
    Infect Immun. 1988 May;56(5):1023-9 PMID: 2895738
  48. Purification of the Escherichia coli type 1 pilin and minor pilus proteins and partial characterization of the adhesin protein.
    J Bacteriol. 1988 Aug;170(8):3350-8 PMID: 2900235
  49. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  50. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase.
    Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767-71 PMID: 3474623
  51. Inhibition of the interaction between fimbrial haemagglutinins and erythrocytes by D-mannose and other carbohydrates.
    J Gen Microbiol. 1972 Jun;71(1):149-57 PMID: 4556971
  52. Transformation of Salmonella typhimurium by plasmid deoxyribonucleic acid.
    J Bacteriol. 1974 Sep;119(3):1072-4 PMID: 4605400
  53. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  54. Mannose-specific adherence of Escherichia coli freshly excreted in the urine of patients with urinary tract infections, and of isolates subcultured from the infected urine.
    Infect Immun. 1981 Dec;34(3):708-11 PMID: 6120897
  55. Role of type 1 fimbriae in the pathogenesis of ascending urinary tract infection induced by escherichia coli in mice.
    Infect Immun. 1983 Mar;39(3):1307-15 PMID: 6132876
  56. Genes of pyelonephritogenic E. coli required for digalactoside-specific agglutination of human cells.
    EMBO J. 1984 May;3(5):1167-73 PMID: 6145590
  57. Identification and characterization of a gene product that regulates type 1 piliation in Escherichia coli.
    J Bacteriol. 1984 Oct;160(1):61-6 PMID: 6148338
  58. Nucleotide sequence of the Tn10 encoded tetracycline resistance gene.
    Nucleic Acids Res. 1983 Jan 25;11(2):525-39 PMID: 6298728
  59. Rapid and reliable protocol for direct sequencing of material amplified by the polymerase chain reaction.
    Biotechniques. 1990 Jul;9(1):66-8, 70, 72 PMID: 2393575
  60. The genetic determinant of adhesive function in type 1 fimbriae of Escherichia coli is distinct from the gene encoding the fimbrial subunit.
    J Bacteriol. 1986 Mar;165(3):1033-6 PMID: 2419305
  61. Type 1 pili are not necessary for colonization of the streptomycin-treated mouse large intestine by type 1-piliated Escherichia coli F-18 and E. coli K-12.
    Infect Immun. 1989 Oct;57(10):3022-9 PMID: 2570752
  62. Protection against Escherichia coli-induced urinary tract infections with hybridoma antibodies directed against type 1 fimbriae or complementary D-mannose receptors.
    Infect Immun. 1985 Jun;48(3):625-8 PMID: 2860067
  63. Gene products specifying adhesion of uropathogenic Escherichia coli are minor components of pili.
    Proc Natl Acad Sci U S A. 1986 Mar;83(6):1891-5 PMID: 2869489
  64. Receptor-binding function of type 1 pili effects bladder colonization by a clinical isolate of Escherichia coli.
    Infect Immun. 1986 Sep;53(3):693-6 PMID: 2875030
  65. Identification and characterization of genes determining receptor binding and pilus length of Escherichia coli type 1 pili.
    J Bacteriol. 1987 Feb;169(2):640-5 PMID: 2879830
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1992-09-00
Pages
5923-35
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC207130
Subset
IM
Grants
NIAID NIH HHS · AI22223 · United States
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