Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1990 May;172(5):2462–2468. doi: 10.1128/jb.172.5.2462-2468.1990

Sequence homology between the subunits of two immunologically and functionally distinct types of fimbriae of Actinomyces spp.

M K Yeung 1, J O Cisar 1
PMCID: PMC208884  PMID: 1970561

Abstract

Nucleotide sequencing of the type 1 fimbrial subunit gene of Actinomyces viscosus T14V revealed a consensus ribosome-binding site followed by an open reading frame of 1,599 nucleotides. The encoded protein of 533 amino acids (Mr = 56,899) was predominantly hydrophilic except for an amino-terminal signal peptide and a carboxy-terminal region identified as a potential membrane-spanning segment. Edman degradation of the cloned protein expressed in Escherichia coli and the type 1 fimbriae of A. viscosus T14V showed that both began with alanine at position 31 of the deduced amino acid sequence. The amino acid compositions of the cloned protein and fimbriae also were comparable and in close agreement with the composition of the deduced protein. The amino acid sequence of the A. viscosus T14V type 1 fimbrial subunit showed no significant global homology with various other proteins, including the pilins of gram-negative bacteria. However, 34% amino acid sequence identity was noted between the type 1 fimbrial subunit of strain T14V and the type 2 fimbrial subunit of Actinomyces naeslundii WVU45 (M. K. Yeung and J. O. Cisar, J. Bacteriol. 170:3803-3809, 1988). This homology included several different conserved sequences of up to eight identical amino acids that were distributed in both the amino- and carboxy-terminal thirds of each Actinomyces fimbrial subunit. These findings indicate that the different types of fimbriae on these gram-positive bacteria share a common ancestry.

Full text

PDF
2462

Selected References

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

  1. Beachey E. H. Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surface. J Infect Dis. 1981 Mar;143(3):325–345. doi: 10.1093/infdis/143.3.325. [DOI] [PubMed] [Google Scholar]
  2. Brennan M. J., Cisar J. O., Sandberg A. L. A 160-kilodalton epithelial cell surface glycoprotein recognized by plant lectins that inhibit the adherence of Actinomyces naeslundii. Infect Immun. 1986 Jun;52(3):840–845. doi: 10.1128/iai.52.3.840-845.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Chou P. Y., Fasman G. D. Prediction of the secondary structure of proteins from their amino acid sequence. Adv Enzymol Relat Areas Mol Biol. 1978;47:45–148. doi: 10.1002/9780470122921.ch2. [DOI] [PubMed] [Google Scholar]
  4. Cisar J. O., Curl S. H., Kolenbrander P. E., Vatter A. E. Specific absence of type 2 fimbriae on a coaggregation-defective mutant of Actinomyces viscosus T14V. Infect Immun. 1983 May;40(2):759–765. doi: 10.1128/iai.40.2.759-765.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cisar J. O., Vatter A. E. Surface fibrils (fimbriae) of Actinomyces viscosus T14V. Infect Immun. 1979 May;24(2):523–531. doi: 10.1128/iai.24.2.523-531.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dayhoff M. O., Barker W. C., Hunt L. T. Establishing homologies in protein sequences. Methods Enzymol. 1983;91:524–545. doi: 10.1016/s0076-6879(83)91049-2. [DOI] [PubMed] [Google Scholar]
  7. 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. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Donkersloot J. A., Cisar J. O., Wax M. E., Harr R. J., Chassy B. M. Expression of Actinomyces viscosus antigens in Escherichia coli: cloning of a structural gene (fimA) for type 2 fimbriae. J Bacteriol. 1985 Jun;162(3):1075–1078. doi: 10.1128/jb.162.3.1075-1078.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Elleman T. C. Pilins of Bacteroides nodosus: molecular basis of serotypic variation and relationships to other bacterial pilins. Microbiol Rev. 1988 Jun;52(2):233–247. doi: 10.1128/mr.52.2.233-247.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fahnestock S. R., Alexander P., Nagle J., Filpula D. Gene for an immunoglobulin-binding protein from a group G streptococcus. J Bacteriol. 1986 Sep;167(3):870–880. doi: 10.1128/jb.167.3.870-880.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fenno J. C., LeBlanc D. J., Fives-Taylor P. Nucleotide sequence analysis of a type 1 fimbrial gene of Streptococcus sanguis FW213. Infect Immun. 1989 Nov;57(11):3527–3533. doi: 10.1128/iai.57.11.3527-3533.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fives-Taylor P. M., Thompson D. W. Surface properties of Streptococcus sanguis FW213 mutants nonadherent to saliva-coated hydroxyapatite. Infect Immun. 1985 Mar;47(3):752–759. doi: 10.1128/iai.47.3.752-759.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. George D. G., Barker W. C., Hunt L. T. The protein identification resource (PIR). Nucleic Acids Res. 1986 Jan 10;14(1):11–15. doi: 10.1093/nar/14.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gerlach G. F., Clegg S. Characterization of two genes encoding antigenically distinct type-1 fimbriae of Klebsiella pneumoniae. Gene. 1988 Apr 29;64(2):231–240. doi: 10.1016/0378-1119(88)90338-1. [DOI] [PubMed] [Google Scholar]
  15. Gibbons R. J., Hay D. I., Cisar J. O., Clark W. B. Adsorbed salivary proline-rich protein 1 and statherin: receptors for type 1 fimbriae of Actinomyces viscosus T14V-J1 on apatitic surfaces. Infect Immun. 1988 Nov;56(11):2990–2993. doi: 10.1128/iai.56.11.2990-2993.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Girard A. E., Jacius B. H. Ultrastructure of Actinomyces viscosus and Actinomyces naeslundii. Arch Oral Biol. 1974 Jan;19(1):71–79. doi: 10.1016/0003-9969(74)90228-3. [DOI] [PubMed] [Google Scholar]
  17. Guss B., Uhlén M., Nilsson B., Lindberg M., Sjöquist J., Sjödahl J. Region X, the cell-wall-attachment part of staphylococcal protein A. Eur J Biochem. 1984 Jan 16;138(2):413–420. doi: 10.1111/j.1432-1033.1984.tb07931.x. [DOI] [PubMed] [Google Scholar]
  18. Handley P. S., Jacob A. E. Some structural and physiological properties of fimbriae of Streptococcus faecalis. J Gen Microbiol. 1981 Dec;127(2):289–293. doi: 10.1099/00221287-127-2-289. [DOI] [PubMed] [Google Scholar]
  19. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  20. Henriksen S. D., Henrichsen J. Twitching motility and possession of polar fimbriae in spreading Streptococcus sanguis isolates from the human throat. Acta Pathol Microbiol Scand B. 1975 Apr;83(2):133–140. doi: 10.1111/j.1699-0463.1975.tb00083.x. [DOI] [PubMed] [Google Scholar]
  21. Hollingshead S. K., Fischetti V. A., Scott J. R. Complete nucleotide sequence of type 6 M protein of the group A Streptococcus. Repetitive structure and membrane anchor. J Biol Chem. 1986 Feb 5;261(4):1677–1686. [PubMed] [Google Scholar]
  22. Klein P., Kanehisa M., DeLisi C. The detection and classification of membrane-spanning proteins. Biochim Biophys Acta. 1985 May 28;815(3):468–476. doi: 10.1016/0005-2736(85)90375-x. [DOI] [PubMed] [Google Scholar]
  23. Klemm P. Fimbrial adhesions of Escherichia coli. Rev Infect Dis. 1985 May-Jun;7(3):321–340. doi: 10.1093/clinids/7.3.321. [DOI] [PubMed] [Google Scholar]
  24. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  25. McIntire F. C., Crosby L. K., Vatter A. E., Cisar J. O., McNeil M. R., Bush C. A., Tjoa S. S., Fennessey P. V. A polysaccharide from Streptococcus sanguis 34 that inhibits coaggregation of S. sanguis 34 with Actinomyces viscosus T14V. J Bacteriol. 1988 May;170(5):2229–2235. doi: 10.1128/jb.170.5.2229-2235.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miller L., Gray L., Beachey E., Kehoe M. Antigenic variation among group A streptococcal M proteins. Nucleotide sequence of the serotype 5 M protein gene and its relationship with genes encoding types 6 and 24 M proteins. J Biol Chem. 1988 Apr 25;263(12):5668–5673. [PubMed] [Google Scholar]
  27. Mizunoe Y., Nakabeppu Y., Sekiguchi M., Kawabata S., Moriya T., Amako K. Cloning and sequence of the gene encoding the major structural component of mannose-resistant fimbriae of Serratia marcescens. J Bacteriol. 1988 Aug;170(8):3567–3574. doi: 10.1128/jb.170.8.3567-3574.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mooi F. R., de Graaf F. K. Molecular biology of fimbriae of enterotoxigenic Escherichia coli. Curr Top Microbiol Immunol. 1985;118:119–138. doi: 10.1007/978-3-642-70586-1_7. [DOI] [PubMed] [Google Scholar]
  29. Paranchych W., Frost L. S. The physiology and biochemistry of pili. Adv Microb Physiol. 1988;29:53–114. doi: 10.1016/s0065-2911(08)60346-x. [DOI] [PubMed] [Google Scholar]
  30. Purcell B. K., Pruckler J., Clegg S. Nucleotide sequences of the genes encoding type 1 fimbrial subunits of Klebsiella pneumoniae and Salmonella typhimurium. J Bacteriol. 1987 Dec;169(12):5831–5834. doi: 10.1128/jb.169.12.5831-5834.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sandberg A. L., Mudrick L. L., Cisar J. O., Brennan M. J., Mergenhagen S. E., Vatter A. E. Type 2 fimbrial lectin-mediated phagocytosis of oral Actinomyces spp. by polymorphonuclear leukocytes. Infect Immun. 1986 Nov;54(2):472–476. doi: 10.1128/iai.54.2.472-476.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Shine J., Dalgarno L. Determinant of cistron specificity in bacterial ribosomes. Nature. 1975 Mar 6;254(5495):34–38. doi: 10.1038/254034a0. [DOI] [PubMed] [Google Scholar]
  34. Staden R. A computer program to enter DNA gel reading data into a computer. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):499–503. doi: 10.1093/nar/12.1part2.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wilbur W. J., Lipman D. J. Rapid similarity searches of nucleic acid and protein data banks. Proc Natl Acad Sci U S A. 1983 Feb;80(3):726–730. doi: 10.1073/pnas.80.3.726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yanagawa R., Honda E. Presence of pili in species of human and animal parasites and pathogens of the genuscorynebacterium. Infect Immun. 1976 Apr;13(4):1293–1295. doi: 10.1128/iai.13.4.1293-1295.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  38. Yeung M. K., Chassy B. M., Cisar J. O. Cloning and expression of a type 1 fimbrial subunit of Actinomyces viscosus T14V. J Bacteriol. 1987 Apr;169(4):1678–1683. doi: 10.1128/jb.169.4.1678-1683.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Yeung M. K., Cisar J. O. Cloning and nucleotide sequence of a gene for Actinomyces naeslundii WVU45 type 2 fimbriae. J Bacteriol. 1988 Sep;170(9):3803–3809. doi: 10.1128/jb.170.9.3803-3809.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. von Heijne G. How signal sequences maintain cleavage specificity. J Mol Biol. 1984 Feb 25;173(2):243–251. doi: 10.1016/0022-2836(84)90192-x. [DOI] [PubMed] [Google Scholar]

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

RESOURCES