Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1998 Jan;74(1):623–632. doi: 10.1016/S0006-3495(98)77821-X

Bacterial adhesion pili are heterologous assemblies of similar subunits.

E Bullitt 1, L Makowski 1
PMCID: PMC1299415  PMID: 9449363

Abstract

P-pili on uropathogenic bacteria are 68-A-diameter rods typically 1 microm in length. These structures project from the outer membrane of Escherichia coli, and contain on their distal tip a thin fibrillum, 25 A in diameter and 150 A long, displaying an adhesin protein responsible for the binding of the bacterium to the surface of epithelial cells lining the urinary tract. Operationally, it is possible to identify three morphologically distinct states of the 68-A-diameter P-pili rods, based on the degree of curvature each can adopt. These states are designated "straight," "curved," and "highly curved." The rods can also be unwound to form thin "threads" that are very similar to the tip fibrillae. Electron microscope data are used to distinguish among these four morphological states and to define limits on the shapes of the pilus proteins. The mechanical properties of the PapA polymers are assessed, and implications of rod polymorphism for pilus function are discussed. A wide variety of data are considered in light of the possibility that all pilins are similar in molecular architecture, with specific differences designed to optimize their specialized functions in the pilus assembly.

Full Text

The Full Text of this article is available as a PDF (483.6 KB).

Selected References

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

  1. Bednar J., Furrer P., Katritch V., Stasiak A. Z., Dubochet J., Stasiak A. Determination of DNA persistence length by cryo-electron microscopy. Separation of the static and dynamic contributions to the apparent persistence length of DNA. J Mol Biol. 1995 Dec 8;254(4):579–594. doi: 10.1006/jmbi.1995.0640. [DOI] [PubMed] [Google Scholar]
  2. Bullitt E., Jones C. H., Striker R., Soto G., Jacob-Dubuisson F., Pinkner J., Wick M. J., Makowski L., Hultgren S. J. Development of pilus organelle subassemblies in vitro depends on chaperone uncapping of a beta zipper. Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):12890–12895. doi: 10.1073/pnas.93.23.12890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bullitt E., Makowski L. Structural polymorphism of bacterial adhesion pili. Nature. 1995 Jan 12;373(6510):164–167. doi: 10.1038/373164a0. [DOI] [PubMed] [Google Scholar]
  4. Båga M., Norgren M., Normark S. Biogenesis of E. coli Pap pili: papH, a minor pilin subunit involved in cell anchoring and length modulation. Cell. 1987 Apr 24;49(2):241–251. doi: 10.1016/0092-8674(87)90565-4. [DOI] [PubMed] [Google Scholar]
  5. Båga M., Normark S., Hardy J., O'Hanley P., Lark D., Olsson O., Schoolnik G., Falkow S. Nucleotide sequence of the papA gene encoding the Pap pilus subunit of human uropathogenic Escherichia coli. J Bacteriol. 1984 Jan;157(1):330–333. doi: 10.1128/jb.157.1.330-333.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chen G. T., Inouye M. Role of the AGA/AGG codons, the rarest codons in global gene expression in Escherichia coli. Genes Dev. 1994 Nov 1;8(21):2641–2652. doi: 10.1101/gad.8.21.2641. [DOI] [PubMed] [Google Scholar]
  7. Chothia C. Structural invariants in protein folding. Nature. 1975 Mar 27;254(5498):304–308. doi: 10.1038/254304a0. [DOI] [PubMed] [Google Scholar]
  8. Denich K., Blyn L. B., Craiu A., Braaten B. A., Hardy J., Low D. A., O'Hanley P. D. DNA sequences of three papA genes from uropathogenic Escherichia coli strains: evidence of structural and serological conservation. Infect Immun. 1991 Nov;59(11):3849–3858. doi: 10.1128/iai.59.11.3849-3858.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dodson K. W., Jacob-Dubuisson F., Striker R. T., Hultgren S. J. Outer-membrane PapC molecular usher discriminately recognizes periplasmic chaperone-pilus subunit complexes. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3670–3674. doi: 10.1073/pnas.90.8.3670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dubochet J., Adrian M., Chang J. J., Homo J. C., Lepault J., McDowall A. W., Schultz P. Cryo-electron microscopy of vitrified specimens. Q Rev Biophys. 1988 May;21(2):129–228. doi: 10.1017/s0033583500004297. [DOI] [PubMed] [Google Scholar]
  11. Egelman E. H., Stasiak A. Structure of helical RecA-DNA complexes. Complexes formed in the presence of ATP-gamma-S or ATP. J Mol Biol. 1986 Oct 20;191(4):677–697. doi: 10.1016/0022-2836(86)90453-5. [DOI] [PubMed] [Google Scholar]
  12. Finer-Moore J., Stroud R. M., Prescott B., Thomas G. J., Jr Subunit secondary structure in filamentous viruses: predictions and observations. J Biomol Struct Dyn. 1984 Aug;2(1):93–100. doi: 10.1080/07391102.1984.10507549. [DOI] [PubMed] [Google Scholar]
  13. Fukami A., Adachi K. A new method of preparation of a self-perforated micro plastic grid and its application. J Electron Microsc (Tokyo) 1965;14(2):112–118. [PubMed] [Google Scholar]
  14. Gittes F., Mickey B., Nettleton J., Howard J. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J Cell Biol. 1993 Feb;120(4):923–934. doi: 10.1083/jcb.120.4.923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gong M., Makowski L. Helical structure of P pili from Escherichia coli. Evidence from X-ray fiber diffraction and scanning transmission electron microscopy. J Mol Biol. 1992 Dec 5;228(3):735–742. doi: 10.1016/0022-2836(92)90860-m. [DOI] [PubMed] [Google Scholar]
  16. Jacob-Dubuisson F., Heuser J., Dodson K., Normark S., Hultgren S. Initiation of assembly and association of the structural elements of a bacterial pilus depend on two specialized tip proteins. EMBO J. 1993 Mar;12(3):837–847. doi: 10.1002/j.1460-2075.1993.tb05724.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jones C. H., Pinkner J. S., Roth R., Heuser J., Nicholes A. V., Abraham S. N., Hultgren S. J. FimH adhesin of type 1 pili is assembled into a fibrillar tip structure in the Enterobacteriaceae. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2081–2085. doi: 10.1073/pnas.92.6.2081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kishchenko G., Makowski L. Shuffling of structural elements in filamentous bacteriophages. Proteins. 1997 Mar;27(3):405–409. doi: 10.1002/(sici)1097-0134(199703)27:3<405::aid-prot8>3.0.co;2-b. [DOI] [PubMed] [Google Scholar]
  19. Kuehn M. J., Heuser J., Normark S., Hultgren S. J. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature. 1992 Mar 19;356(6366):252–255. doi: 10.1038/356252a0. [DOI] [PubMed] [Google Scholar]
  20. Lindberg F., Lund B., Normark S. Gene products specifying adhesion of uropathogenic Escherichia coli are minor components of pili. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1891–1895. doi: 10.1073/pnas.83.6.1891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lund B., Lindberg F., Marklund B. I., Normark S. The PapG protein is the alpha-D-galactopyranosyl-(1----4)-beta-D-galactopyranose-binding adhesin of uropathogenic Escherichia coli. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5898–5902. doi: 10.1073/pnas.84.16.5898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Normark S., Lark D., Hull R., Norgren M., Båga M., O'Hanley P., Schoolnik G., Falkow S. Genetics of digalactoside-binding adhesin from a uropathogenic Escherichia coli strain. Infect Immun. 1983 Sep;41(3):942–949. doi: 10.1128/iai.41.3.942-949.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Oosawa F. The flexibility of F-actin. Biophys Chem. 1980 Jun;11(3-4):443–446. doi: 10.1016/0301-4622(80)87021-9. [DOI] [PubMed] [Google Scholar]
  24. Orlova A., Egelman E. H. A conformational change in the actin subunit can change the flexibility of the actin filament. J Mol Biol. 1993 Jul 20;232(2):334–341. doi: 10.1006/jmbi.1993.1393. [DOI] [PubMed] [Google Scholar]
  25. Parge H. E., Forest K. T., Hickey M. J., Christensen D. A., Getzoff E. D., Tainer J. A. Structure of the fibre-forming protein pilin at 2.6 A resolution. Nature. 1995 Nov 2;378(6552):32–38. doi: 10.1038/378032a0. [DOI] [PubMed] [Google Scholar]
  26. Rivetti C., Guthold M., Bustamante C. Scanning force microscopy of DNA deposited onto mica: equilibration versus kinetic trapping studied by statistical polymer chain analysis. J Mol Biol. 1996 Dec 20;264(5):919–932. doi: 10.1006/jmbi.1996.0687. [DOI] [PubMed] [Google Scholar]
  27. Smith S. B., Cui Y., Bustamante C. Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science. 1996 Feb 9;271(5250):795–799. doi: 10.1126/science.271.5250.795. [DOI] [PubMed] [Google Scholar]
  28. Solovyev V. V., Salamov A. A. Predicting alpha-helix and beta-strand segments of globular proteins. Comput Appl Biosci. 1994 Dec;10(6):661–669. doi: 10.1093/bioinformatics/10.6.661. [DOI] [PubMed] [Google Scholar]
  29. Takebayashi T., Morita Y., Oosawa F. Electronmicroscopic investigation of the flexibility of F-actin. Biochim Biophys Acta. 1977 Jun 24;492(2):357–363. doi: 10.1016/0005-2795(77)90086-1. [DOI] [PubMed] [Google Scholar]
  30. Uhlin B. E., Norgren M., Båga M., Normark S. Adhesion to human cells by Escherichia coli lacking the major subunit of a digalactoside-specific pilus-adhesin. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1800–1804. doi: 10.1073/pnas.82.6.1800. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES