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An analysis of the organization and evolution of type 4 fimbrial (MePhe) subunit proteins

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Summary

We have analyzed and compared the amino acid sequences of the type 4 fimbrial subunits fromPseudomonas aeruginosa, Moraxella bovis, M. nonliquefaciens, Bacteroides nodosus, Neisseria gonorrhoeae, andN. meningitidis. We propose a consensus sequence for the highly conserved aminoterminal regions of these proteins. In the variable regions, a domain corresponding to an epitope common toN. gonorrhoeae andN. meningitidis fimbriae is conserved, both in sequence and in environment, in fimbrial subunits fromB. nodosus. The subunits fromM. bovis andP. aeruginosa do not show any homologies to this sequence. In all of the subunits, the carboxy-terminal half of the molecule consists of a series of fairly hydrophobic domains. The last three domains, two of which include the cysteines of the disulfide bridge inN. gonorrhoeae, P. aeruginosa, andM. bovis, are more or less conserved in sequence in all of the proteins including that ofB. nodosus. We propose that these conserved hydrophobic regions, which have the potential to form a series of beta-sheets, form a structural framework around which more variable hydrophilic sequences determining immunological profile are arranged. The evolutionary relationships of the contemporary proteins and the distribution of type 4 fimbriae are also discussed.

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References

  • Anderson BJ, Kristo CL, Egerton JR, Mattick JS (1986) Variation in the structural subunits and basal protein antigens ofBacteroides nodosus fimbriae. J Bacteriol 166:453–460.

    PubMed  Google Scholar 

  • Bovre K (1970) Pulse-RNA-DNA hybridization between rodshaped and coccal species of theMoraxella-Neisseria groups. Acta Pathol Microbiol Scand Sect B Microbiol 78:565–574

    Google Scholar 

  • Bovre K (1984) Neisseriaceae. In: Kreig NR, Holt JG (eds) Bergey's manual of systematic bacteriology. Williams and Wilkins, Baltimore, p 288

    Google Scholar 

  • Bradley DE (1980) A function ofPseudomonas aeruginosa PAO pili: twitching motility. Can J Microbiol 26:146–154

    PubMed  Google Scholar 

  • Bradley DE, Pitt TL (1975) An immunological study of the pili ofPseudomonas aeruginosa. J Hyg Camb 74:419–430

    PubMed  Google Scholar 

  • Brinton CC, Bryan J, Dillon JA, Guerina N, Jacobson LJ, Labik A, Lee S, Levine A, Lim S, McMichael J, Polen S, Rogers K, To AC-C, To SC-M (1978) Uses of pili in gonorrhea control: role of bacterial pili in disease, purification and properties of gonococcal pili, and progress in the development of a gonococcal pilus vaccine for gonorrhea. In: Brooks GF, Gotschlich EC, Holmes KK, Sawyer WS, Young FE (eds) Immunobiology ofNeisseria gonorrhoeae. American Society for Microbiology, Washington DC, p 155

    Google Scholar 

  • Buchanan TM (1975) Antigenic heterogeneity of gonococcal pili. J Exp Med 141:1470–1475

    PubMed  Google Scholar 

  • Dayhoff MO, Schwartz RM, Orcutt BC (1978) A model of evolutionary change in proteins. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5, National Biomedical Research Foundation, Washington DC, p 345

    Google Scholar 

  • Elleman TC, Hoyne PA (1984) Nucleotide sequence of the gene encoding pilin ofBacteroides nodosus, the causal organism of ovine footrot. J Bacteriol 160:1184–1187

    PubMed  Google Scholar 

  • Elleman TC, Hoyne PA, McKern NM, Stewart DJ (1986) Nucleotide sequence of the gene encoding the two-subunit pilin ofBacteroides nodosus 265. J Bacteriol 167:243–250

    PubMed  Google Scholar 

  • Engelman DM, Steitz TA (1981) The spontaneous insertion of proteins into and across membranes: the helical hairpin hypothesis. Cell 23:411–422

    PubMed  Google Scholar 

  • Every D, Skerman TM (1982) Protection of sheep against experimental footrot by vaccination with pili purified fromBacteroides nodosus. NZ Vet J 30:156–158

    Google Scholar 

  • Finlay BB, Pasloske BL, Paranchych W (1986) Expression of thePseudomonas aeruginosa PAK pilin gene inEscherichia coli. J Bacteriol 165:625–630

    PubMed  Google Scholar 

  • Folkhard W, Marvin DA, Watts TH, Paranchych W (1981) Structure of polar pili fromPseudomonas aeruginosa strains K and O. J Mol Biol 149:79–93

    PubMed  Google Scholar 

  • Fontaine EAR, Borriello SP, Taylor-Robinson D, Davies HA (1984) Differential characteristics of a small gram-negative anaerobe associated with non-gonococcal urethritis which morphologically resemblesBacteroides ureolyticus. Scand J Urol Nephrol Suppl 86:157–165

    Google Scholar 

  • Froholm LO, Bovre K (1972) Fim briation associated with the spreading-corroding colony type inMoraxella kingii. Acta Pathol Microbiol Scand Sect B Microbiol 80:641–648

    Google Scholar 

  • Froholm LO, Sletten K (1977) Purification and N-terminal sequence of a fimbrial protein fromMoraxella nonliquefaciens. FEBS Lett 73:29–32

    PubMed  Google Scholar 

  • Frost LS, Carpenter M, Paranchych W (1978) N-methylphenylalanine at the N-terminus of pilin isolated fromPseudomonas aeruginosa K. Nature 271:87–89

    PubMed  Google Scholar 

  • Haas R, Meyer TF (1986) The repertoire of silent pilus genes inNeisseria gonorrhoeae: evidence for gene conversion. Cell 44:107–115

    PubMed  Google Scholar 

  • Hagblom P, Segal E, Billyard E, So M (1985) Infragenic recombination leads to pilus antigenic variation inNeisseria gonorrhoeae. Nature 315:156–158

    PubMed  Google Scholar 

  • Henrichsen J (1975) The occurrence of twitching motility among gram-negative bacteria. Acta Pathol Microbiol Scand Sect B Microbiol 83:171–178

    Google Scholar 

  • Henrichsen J (1983) Twitching motility. Annu Rev Microbiol 37:81–93

    PubMed  Google Scholar 

  • Henrichsen J, Blom J (1975) Examination of fimbriation of some gram-negative rods with and without twitching and gliding motility. Acta Pathol Microbiol Scand Sect B Microbiol 83:161–170

    Google Scholar 

  • Henrichsen J, Froholm LO, Bovre K (1972) Studies on bacterial surface translocation 2. Correlation of twitching motility and fimbriation in colony variants ofMoraxella nonliquefaciens, M. bovis andM. kingii. Acta Pathol Microbiol Scand Sect B Microbiol 80:445–452

    Google Scholar 

  • Henriksen SD, Froholm LO (1975) A fimbriated strain ofPasteurella multocida with spreading and corroding colonies. Acta Pathol Microbiol Scand Sect B Microbiol 83:129–132

    Google Scholar 

  • Henriksen SD, Henrichsen J (1975) Twitching motility and possession of polar fimbriae in spreadingStreptococcus sanguis isolates from the human throat. Acta Pathol Microbiol Scand Sect B Microbiol 83:133–140

    Google Scholar 

  • Hermodson MA, Chen KCS, Buchanan TM (1978)Neisseria pili proteins: amino-terminal amino acid sequences and identification of an unusual amino acid. Biochemistry 17:442–445

    PubMed  Google Scholar 

  • Jones GW, Isaacson RE (1983) Proteinaceous bacterial adhesins and their receptors. Int Rev Microbiol 10:229–260

    Google Scholar 

  • Kanehisa M, Klein P, Greif P, DeLisi C (1984) Computer analysis and structure prediction of nucleic acids and proteins. Nucleic Acids Res 12:417–428

    PubMed  Google Scholar 

  • Kingshury DT, Fanning GR, Johnson KE, Brenner DJ (1969) Thermal stability of interspeciesNeisseria DNA duplexes. J Gen Microbiol 55:201–208

    PubMed  Google Scholar 

  • Kyte J, Doolittle RE (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    PubMed  Google Scholar 

  • Lambden PR, Robertson JN, Watt PJ (1980) Biological properties of two distinct pilus types produced by isogenic variants ofNeisseria gonorrhoeae P9. J Bacteriol 141:393–396

    PubMed  Google Scholar 

  • Love DN, Jones RF, Bailey M, Calverley A (1984) Comparison of strains of gram-negative, anaerobic, agar-corroding rods isolated from soft tissue infections in cats and dogs with type strains ofBacteroides gracilis, Wolinella recta, Wolinella succinogenes andCampylobacter concisus. J Clin Microbiol 20:747–750

    PubMed  Google Scholar 

  • Marrs CF, Schoolnik G, Koomey JM, Hardy J, Rothbard J, Falkow S (1985) Cloning and sequencing of aMoraxella bovis pilin gene. J Bacteriol 163:132–139

    PubMed  Google Scholar 

  • Mattick JS, Bills MM, Anderson BJ, Dalrymple B, Mott MR, Egerton JR (1987) Morphogenetic expression ofBacteroides nodosus fimbriae inPseudomonas aeruginosa. J Bacteriol 169:33–41

    PubMed  Google Scholar 

  • McKern NM, O'Donnell IJ, Inglis AS, Stewart DJ, Clark BL (1983) Amino acid sequence of pilin fromBacteroides nodosus (strain 198), the causative agent of ovine footrot. FEBS Lett 164:149–153

    PubMed  Google Scholar 

  • McKern NM, O'Donnell IJ, Stewart DJ, Clark BL (1985) Primary structure of pilin protein fromBacteroides nodosus strain 216: comparison with corresponding protein from strain 198. J Gen Microbiol 131:1–6

    PubMed  Google Scholar 

  • Meyer TF, Billyard E, Haas R, Storzbach S, So M (1984) Pilus genes ofNeisseria gonorrheae: chromosomal organization and DNA sequence. Proc Natl Acad Sci USA 81:6110–6114

    PubMed  Google Scholar 

  • Novotny J, Auffray C (1984) A program for prediction of protein secondary structure from nucleotide sequence data: application to histocompatibility antigens. Nucleic Acids Res 12:243–255

    PubMed  Google Scholar 

  • Olafson RW, McCarthy PJ, Bhatti AR, Dooley JSG, Heckels JE, Trust TJ (1985) Structural and antigenic analysis of meningococcal piliation. Infect Immun 48:336–342

    PubMed  Google Scholar 

  • Ottow JCG (1975) Ecology, physiology, and genetics of fimbriae and pili. Annu Rev Microbiol 29:79–108

    PubMed  Google Scholar 

  • Palleroni NJ, Kunisawa R, Contopoulou R, Doudoroff M (1973) Nucleic acid homologies in the genusPseudomonas. Int J Syst Bacteriol 23:333–339

    Google Scholar 

  • Paranchych W, Frost LS, Carpenter M (1978) N-terminal amino acid sequence of pilin isolated fromPseudomonas aeruginosa. J Bacteriol 134:1179–1180

    PubMed  Google Scholar 

  • Pugh GW, Hughes DE, Booth GD (1977) Experimentally induced infectious bovine keratonconjunctivitis: effectiveness of a pilus vaccine against exposure to homologus strains ofMoraxella bovis. Am J Vet Res 38:1519–1522

    PubMed  Google Scholar 

  • Reisner AH, Bucholtz CA (1986) The MTX package of computer programmes for the comparison of sequences of nucleotides and amino acid residues. Nucleic Acids Res 14:233–238

    PubMed  Google Scholar 

  • Rothbard JB, Fernandez R, Schoolnik GK (1984) Strain-specific and common epitopes of gonococcal pili. J Exp Med 160: 208–221

    PubMed  Google Scholar 

  • Rothbard JB, Fernandez R, Wang L, Teng NNH, Schoolnik GK (1985) Antibodies to peptides corresponding to a conserved sequence of gonococcal pilins block bacterial adhesion. Proc Natl Acad Sci USA 82:915–919

    PubMed  Google Scholar 

  • Sandhu TS, White FH, Simpson CF (1974) Association of pili with rough colony type ofMoraxella bovis. Am J Vet Res 35:437–439

    PubMed  Google Scholar 

  • Sastry PA, Finlay BB, Pasloske BL, Paranchych W, Pearlstone JR, Smillie LB (1985a) Comparative studies of the amino acid and nucleotide sequences of pilin derived fromPseudomonas aeruginosa PAK and PAO. J Bacteriol 164:571–577

    PubMed  Google Scholar 

  • Sastry PA, Pearlstone JR, Smillie LB, Paranchych W (1985b) Studies on the primary structure and antigenic determinants of pilin isolated fromPseudomonas aeruginosa K. Can J Biochem Cell Biol 63:284–291

    PubMed  Google Scholar 

  • Schoolnik GK, Tai JY, Gotschlich EC (1983) A pilus peptide vaccine for the prevention of gonorrhea. Prog Allergy 33:314–331

    PubMed  Google Scholar 

  • Schoolnik GK, Fernandez R, Tai JY, Rothbard J, Gotschlich EC (1984) Gonococcal pili primary structure and receptor binding domain. J Exp Med 159:1351–1370

    PubMed  Google Scholar 

  • Segal E, Hagblom P, Seifert HS, So M (1986) Antigenic variation of gonococcal pilus involves assembly of separated silent gene segments. Proc Natl Acad Sci USA 83:2177–2181

    PubMed  Google Scholar 

  • Shah HN, Collins MD (1983) GenusBacteroides. A chemotaxonomical perspective. J Appl Bacteriol 55:403–416

    PubMed  Google Scholar 

  • Stephens DS, Whitney AM, Rothbard J, Schoolnik GK (1985) Pili ofNeisseria meningitidis: analysis of structure and investigation of structural and antigenic relationships to gonococcal pili. J Exp Med 161:1539–1553

    PubMed  Google Scholar 

  • Tanner ACR, Badger S, Lai CH, Listgarten MA, Visconti RA, Socransky SS (1981)Wolinella gen. nov.,Wolinella succinogenes (Vibrio succinogenes Wolin et al.) comb. nov., and description ofBacteroides gracilis sp. nov.,Wolinella recta sp. nov.,Campylobacter concisius sp. nov., andEikenella corrodens from humans with periodontal disease. Int J Syst Bacteriol 31:432–445

    Google Scholar 

  • Tanner ACR, Listgarten MA, Ebersole JL (1984)Wolinella curva sp. nov.: “Vibrio succinogenes” of human origin. Int J Syst Bacteriol 34:275–282

    Google Scholar 

  • Virji M, Heckels JE (1983) Antigenic cross-reactivity ofNeisseria pili: investigations with type-and species-specific monoclonal antibodies. J Gen Microbiol 129:2761–2768

    PubMed  Google Scholar 

  • Watts TH, Kay CM, Paranchych W (1982) Dissociation and characterization of pilin isolated fromPseudomonas aeruginosa strains PAK and PAO. Can J Biochem 60:867–872

    PubMed  Google Scholar 

  • Watts TH, Kay CM, Paranchych W (1983) Spectral properties of three quaternary arrangements ofPseudomonas pilin. Biochemistry 22:3640–3646

    PubMed  Google Scholar 

  • Woese CR, Weisburg WG, Paster BJ, Hahn CM, Tanner RS, Krieg NR, Koops HP, Harms H, Stackebrandt E (1984) The phylogeny of the purple bacteria: the beta subdivision. Syst Appl Microbiol 5:327–336

    Google Scholar 

  • Woese CR, Weisburg WG, Hahn CM, Paster BJ, Zablen LB, Lewis BJ, Macke TJ, Ludwig W, Stackebrandt E (1985) The phylogeny of the purple bacteria: the gamma subdivision. Syst Appl Microbiol 6:25–33

    Google Scholar 

  • Woods DE, Straus DC, Johanson WG Jr, Berry VK, Bass JA (1980) Role of pili in adherence ofPseudomonas aeruginosa to mammalian buccal epithelial cells. Infect Immun 29:1146–1151

    PubMed  Google Scholar 

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Dalrymple, B., Mattick, J.S. An analysis of the organization and evolution of type 4 fimbrial (MePhe) subunit proteins. J Mol Evol 25, 261–269 (1987). https://doi.org/10.1007/BF02100020

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