1887

Microbiology Society logo

Volume 144, Issue 12

The 35 kDa iron-regulated protein is an FbpA homologue Free

Abstract

Summary: In a previous investigation, a 35 kDa iron-regulated protein was identified from total cellular proteins of grown under iron-depleted conditions. This study reports identification of the gene encoding the 35 kDa protein based on complementation of an strain transformed with a plasmid derived from a lambda ZAP II library. Cross-reactivity was demonstrated between an anti-35 kDa mAb and a 35 kDa protein expressed in this strain. Furthermore, a translated ORF identified on the recombinant plasmid corresponded with the N-terminal amino acid sequence of the intact and a CNBr-cleaved fragment of the 35 kDa iron-regulated protein. Nucleotide sequence analysis of the gene encoding the 35 kDa protein demonstrated homology with the cluster 1 group of extracellular solute-binding proteins, especially to the iron-binding proteins of this family. Complete sequence analysis of the recombinant plasmid insert identified three other predominant ORFs, two of which appeared to be in an operonic organization with These latter components ( and ) showed homology to the transmembrane and ATPase components of ATP-binding cassette (ABC)-type uptake systems, respectively. Based on amino acid/DNA sequencing, citrate competition assay of iron affinity and visible wavelength spectra, it was concluded that the 35 kDa protein functions as an FbpA homologue (referred to as PFbpA) and that the gene encoding this protein is part of an operon comprising a member of the FbpABC family of iron uptake systems. Primary sequence analysis revealed rather surprisingly that PFbpA is more closely related to the intracellular Mn/Febinding protein IdiA found in cyanobacteria than to any of the homologous FbpA proteins currently known in commensal or pathogenic members of the or .

  • Published Online:
Keyword(s): ABC transporter , FbpA , iron and Pasteurella baemolytica
Society for General Microbiology 1998
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-144-12-3425
1998-12-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/144/12/mic-144-12-3425.html?itemId=/content/journal/micro/10.1099/00221287-144-12-3425&mimeType=html&fmt=ahah

References

  1. Adhikari P., Kirby S.D., Nowalk A.J., Veraldi K.L., Schryvers A.B., Mietzner T.A. 1995; Biochemical characterization of a Haemophilus influenzae periplasmic iron transport operon.. J Biol Chem 42:25142–25149
     [Google Scholar]
  2. Adhikari P., Berish S.A., Nowalk A.J., Veraldi K.L., Morse S.A., Mietzner T.A. 1996; The fbpABC locus of Neisseria gonorrhoeae functions in the periplasm-to-cytosol transport of iron.. J Bacteriol 178:2145–2149
     [Google Scholar]
  3. Angerer A., Gaisser S., Braun V. 1990; Nucleotide sequences of the sfuA, sfuB and sfuC genes of Serratia marcescens suggest a periplasmic-binding-protein-dependant iron transport mechanism.. J Bacteriol 172:572–578
     [Google Scholar]
  4. Berish S. A., Kapczynski D. R., Morse S. A. 1990a; Nucleotide sequence of the Fbp gene from Neisseria meningitidis. . Nucleic Acids Res 18:4596
     [Google Scholar]
  5. Berish S. A., Mietzner T. A., Mayer L. W., Genco C. A., Holloway B. P., Morse S. A. 1990b; Molecular cloning and characterization of the structural gene for the major iron regulated protein expressed by Neisseria gonorrhoeae. . J Exp Med 171:1535–1546
     [Google Scholar]
  6. Berish S.A., Chen C.-Y., Mietzner T.A., Morse S.A. 1992; Expression of a functional neisserial fbp gene in Escherichia coli. . Mol Microbiol 6:2607–2615
     [Google Scholar]
  7. Burland V., Plunkett G. III Sofia H.J., Daniels D.L., Blattner F.R. 1995; Analysis of the Escherichia coli genome. VI. DNA sequence of the region from 92·8 through 100 minutes.. Nucleic Acids Res 23:2105–2119
     [Google Scholar]
  8. Bruns C.M., Nowalk A.J., Arvai A.S., McTigue M.A., Vaughan K.G., Mietzner T.A., McRee D.E. 1997; Structure of Haemophilus influenzae Fe( + 3)-binding protein reveals convergent evolution within a superfamily.. Nat Struct Biol 4:919–924
     [Google Scholar]
  9. Chen C.-Y., Berish S.A., Morse S.A., Mietzner T.A. 1993; The ferric iron-binding protein of pathogenic Neisseria spp. functions as a periplasmic transport protein in iron acquisition from human transferrin.. Mol Microbiol 10:311–318
     [Google Scholar]
  10. Chin N., Frey J., Chang C., Chang Y. 1996; Identification of a locus involved in the utilization of iron by Actinobacillus pleuropneumoniae. . FEMS Microbiol Lett 143:1–6
     [Google Scholar]
  11. Deneer H.G., Potter A.A. 1989; Iron-repressible outer- membrane proteins of Pasteurella haemolytica. . J Gen Microbiol 135:435–443
     [Google Scholar]
  12. Eick-Helmerich K., Hantke K., Braun V. 1987; Cloning and expression of the exbB gene of Escherichia coli K-12.. Mol Gen Genet 206:246–251
     [Google Scholar]
  13. Genco C.A., Berish S.A., Chen C.-Y., Morse S., Trees D.L. 1994; Genetic diversity of the iron-binding protein (Fbp) gene of the pathogenic and commensal Neisseria. . FEMS Microbiol Lett 116:123–130
     [Google Scholar]
  14. Gomez J. A., Agra C., Ferron L., Powell N., Pintor M., Criado M.T., Ferreiros C.M. 1996; Antigenicity, cross-reactivity and surface exposure of the Neisseria meningitidis 37 kDa protein (Fbp).. Vaccine 14:1340–1346
     [Google Scholar]
  15. Gray-Owen S.D., Schryvers A.B. 1996; Bacterial transferrin and lactoferrin receptors.. Trends Microbiol 4:185–191
     [Google Scholar]
  16. Harkness R.E., Chong P., Klein M.H. 1992; Identification of two iron-repressed periplasmic proteins in Haemophilus influenzae. . J Bacteriol 174:2425–2430
     [Google Scholar]
  17. Higgins C.F. 1992; ABC transporters: from microorganisms to man.. Annu Rev Cell Biol 8:67–113
     [Google Scholar]
  18. Higgins D.G., Thompson J.D., Gibson T.J. 1996; Using clustal for multiple sequence alignments.. Methods Enzymol 266:383–402
     [Google Scholar]
  19. Innis M.A., Gelfand D.H. 1990 PCR Protocols: a Guide to Methods and Applications pp. 3–12 Innis M. A., Gelfand D. H., Sninsky J. J., White T. J. Edited by San Diego:: Academic Press.;
     [Google Scholar]
  20. Kaneko T., Tanaka A., Sato S., Kotani H., Sazuka T., Miyajima N., Sugiura M., Tabata S. 1995; Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. I. Sequence features in the 1 Mb region from map positions 64% to 92% of the genome.. DNA Res 2:153–166
     [Google Scholar]
  21. Khun H., Kirby S.D., Lee B.C. 1998; A Neisseria meningitidis fbp ABC mutant is incapable of using nonheme iron for growth.. Infect Immun 66:2330–2336
     [Google Scholar]
  22. Kirby S.D., Gray-Owen S.D., Schryvers A.B. 1997; Characterization of a ferric-binding protein mutant in Haemophilus influenzae. . Mol Microbiol 25:979–987
     [Google Scholar]
  23. Klaus-Peter M., Thole H. H., Pistorius E. K. 1996; IdiA, a 34 kDa protein in the cyanobacteria Synechococcus sp. strains PCC 6301 and PCC 7942, is required for growth under iron and manganese limitations.. Microbiology 142:2635–2645
     [Google Scholar]
  24. Laemmli U.K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4.. Nature 227:680–685
     [Google Scholar]
  25. Lainson F.A., Harkins D.C., Wilson C.F., Sutherland A.D., Murray J.E., Donachie W., Baird G.D. 1991; Identification and localization of an iron-regulated 35 kDa protein of Pasteurella haemolytica serotype A2.. J Gen Microbiol 137:219–226
     [Google Scholar]
  26. Liss L.R. 1987; New M13 host: DH5α F′ competent cells.. BRL Focus 9:13
     [Google Scholar]
  27. Mietzner T.A., Morse S.A. 1994; The role of iron-binding proteins in the survival of pathogenic bacteria.. Annu Rev Nutr 14:471–493
     [Google Scholar]
  28. Mosier D.A., Simons K.R., Confer A.W., Panciera R.J., Clinkenbeard K.D. 1989; Pasteurella haemolytica antigens associated with resistance to pneumonic pasteurellosis.. Infect Immun 57:711–716
     [Google Scholar]
  29. Murray J.E., Davies R.C., Lainson F.A., Wilson C.F., Donachie W. 1992; Antigenic analysis of iron-regulated proteins in Pasteurella haemolyticaA and T biotypes by immunoblotting reveals biotype-specific epitopes.. J Gen Microbiol 138:283–288
     [Google Scholar]
  30. Ogunnariwo J.A., Schryvers A.B. 1990; Iron acquisition in Pasteurella haemolytica: expression and identification of a bovine-specific transferrin receptor.. Infect Immun 58:2091–2097
     [Google Scholar]
  31. Ogunnariwo J.A., Woo T.K.W., Lo R.Y.C., Gonzalez G.C., Schryvers A.B. 1997; Characterization of the Pasteurella haemolytica transferrin receptor genes and the recombinant receptor proteins.. Microb Pathog 23:273–284
     [Google Scholar]
  32. Riggs P. 1994; Expression and purification of maltose binding protein fusions 16-6-1 to 16-6-14. In Current Protocols in Molecular Biology pp. 2 Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J.A., Struhl K. Edited by New York:: Wiley;
     [Google Scholar]
  33. Sambrook J., Fritsch E.F., Maniatis T. 1989 Molecular Cloning-, a Laboratory Manual, 2nd. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory.;
     [Google Scholar]
  34. Sanders J.D., Cope L.D., Hansen E.J. 1994; Identification of a locus involved in the utilization of iron by Haemophilus influenzae. . Infect Immun 62:4515–4525
     [Google Scholar]
  35. Saurin W., Küster W., Dassa E. 1994; Bacterial binding protein-dependent permeases: characterization of distinctive signatures for functionally related integral cytoplasmic membrane proteins.. Mol Microbiol 12:993–1004
     [Google Scholar]
  36. Schryvers A.B., Gonzalez G.C. 1990; Receptors for transferrin in pathogenic bacteria are specific for the host's protein.. Can J Microbiol 36:145–147
     [Google Scholar]
  37. Schwyn B., Neilands J.B. 1987; Universal chemical assay for the detection and determination of siderophores.. Anal Biochem 160:47–56
     [Google Scholar]
  38. Shine J., Dalgarno L. 1974; The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites.. Proc Nat Acad Sci USA 711342–1346
     [Google Scholar]
  39. Syvanen M. 1994; Horizontal gene transfer: evidence and possible consequences.. Annu Rev Genet 28:237–261
     [Google Scholar]
  40. Tabatabai L.B., Frank G.H. 1997; Purification and characterization of a 31-kilodalton iron regulated periplasmic protein from Pasteurella haemolytica Al.. Prep Biochem Biotechnol 170:253–269
     [Google Scholar]
  41. Tabor S. 1994; Expression using the T7 RNA polymerase/ promoter system, 16-2-1 to 16-2-11. In Current Protocols in Molecular Biology pp. 2 Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K. Edited by New York:: Wiley.;
     [Google Scholar]
  42. Tam R., Saier M.H. Jr 1993; Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria.. Microbiol Rev 57:320–346
     [Google Scholar]
  43. Williamson C.A., Slocum R.D. 1994; Isolation of cDNA clones by complementation of E. coli mutants with infective pBluescript phagemid libraries.. Biotechniques 16:986–988
     [Google Scholar]
  44. Zimmermann L., Angerer A., Braun V. 1989; Mechanistically novel iron (III) transport system inSerratia marcescens. . J Bacteriol 171:238–243
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-144-12-3425
Loading
The Pasteurella haemolytica 35 kDa iron-regulated protein is an FbpA homologue
Microbiology 144, 3425 (1998); https://doi.org/10.1099/00221287-144-12-3425
/content/journal/micro/10.1099/00221287-144-12-3425
/content/journal/micro/10.1099/00221287-144-12-3425
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error