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. 1989 Feb;171(2):1041–1047. doi: 10.1128/jb.171.2.1041-1047.1989

Evolutionary relationship between the TonB-dependent outer membrane transport proteins: nucleotide and amino acid sequences of the Escherichia coli colicin I receptor gene.

C D Nau 1, J Konisky 1
PMCID: PMC209699  PMID: 2644220

Abstract

The nucleotide sequence of the Escherichia coli colicin I receptor gene (cir) has been determined. The predicted mature protein consists of 599 amino acids and has a molecular weight of 67,169. Several previously noted characteristics of other E. coli outer membrane protein sequences were also identified in the sequence of Cir. These include an overall acidic nature, the absence of long hydrophobic stretches of amino acids, and a lack of predicted alpha-helical secondary structure. Because two classes of outer membrane proteins (the TonB-dependent transport proteins and the porins) share some structural features, protein sequences from both of these groups were aligned pairwise and scored for sequence similarity. Statistical evidence suggested that the porins were not related to the proteins in the TonB-dependent group; however, there was a significant relationship between the proteins in the TonB-dependent group. On the basis of the multiple progressive sequence alignment and the similarity scores derived from it, a tree representing evolutionary distance between five TonB-dependent outer membrane transport proteins was generated.

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Selected References

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

  1. Coulton J. W., Mason P., Cameron D. R., Carmel G., Jean R., Rode H. N. Protein fusions of beta-galactosidase to the ferrichrome-iron receptor of Escherichia coli K-12. J Bacteriol. 1986 Jan;165(1):181–192. doi: 10.1128/jb.165.1.181-192.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Coulton J. W., Reid G. K., Campana A. Export of hybrid proteins FhuA'-'LacZ and FhuA'-'PhoA to the cell envelope of Escherichia coli K-12. J Bacteriol. 1988 May;170(5):2267–2275. doi: 10.1128/jb.170.5.2267-2275.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dente L., Cesareni G., Cortese R. pEMBL: a new family of single stranded plasmids. Nucleic Acids Res. 1983 Mar 25;11(6):1645–1655. doi: 10.1093/nar/11.6.1645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Eisenberg D. Three-dimensional structure of membrane and surface proteins. Annu Rev Biochem. 1984;53:595–623. doi: 10.1146/annurev.bi.53.070184.003115. [DOI] [PubMed] [Google Scholar]
  5. Feng D. F., Doolittle R. F. Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J Mol Evol. 1987;25(4):351–360. doi: 10.1007/BF02603120. [DOI] [PubMed] [Google Scholar]
  6. Feng D. F., Johnson M. S., Doolittle R. F. Aligning amino acid sequences: comparison of commonly used methods. J Mol Evol. 1984;21(2):112–125. doi: 10.1007/BF02100085. [DOI] [PubMed] [Google Scholar]
  7. Finer-Moore J., Stroud R. M. Amphipathic analysis and possible formation of the ion channel in an acetylcholine receptor. Proc Natl Acad Sci U S A. 1984 Jan;81(1):155–159. doi: 10.1073/pnas.81.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Garnier J., Osguthorpe D. J., Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol. 1978 Mar 25;120(1):97–120. doi: 10.1016/0022-2836(78)90297-8. [DOI] [PubMed] [Google Scholar]
  9. Griggs D. W., Tharp B. B., Konisky J. Cloning and promoter identification of the iron-regulated cir gene of Escherichia coli. J Bacteriol. 1987 Dec;169(12):5343–5352. doi: 10.1128/jb.169.12.5343-5352.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Grosjean H., Fiers W. Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. Gene. 1982 Jun;18(3):199–209. doi: 10.1016/0378-1119(82)90157-3. [DOI] [PubMed] [Google Scholar]
  11. Heller K. J., Kadner R. J., Günther K. Suppression of the btuB451 mutation by mutations in the tonB gene suggests a direct interaction between TonB and TonB-dependent receptor proteins in the outer membrane of Escherichia coli. Gene. 1988 Apr 15;64(1):147–153. doi: 10.1016/0378-1119(88)90488-x. [DOI] [PubMed] [Google Scholar]
  12. Heller K., Kadner R. J. Nucleotide sequence of the gene for the vitamin B12 receptor protein in the outer membrane of Escherichia coli. J Bacteriol. 1985 Mar;161(3):904–908. doi: 10.1128/jb.161.3.904-908.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Heller K., Mann B. J., Kadner R. J. Cloning and expression of the gene for the vitamin B12 receptor protein in the outer membrane of Escherichia coli. J Bacteriol. 1985 Mar;161(3):896–903. doi: 10.1128/jb.161.3.896-903.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Inokuchi K., Mutoh N., Matsuyama S., Mizushima S. Primary structure of the ompF gene that codes for a major outer membrane protein of Escherichia coli K-12. Nucleic Acids Res. 1982 Nov 11;10(21):6957–6968. doi: 10.1093/nar/10.21.6957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kennedy S. J. Structures of membrane proteins. J Membr Biol. 1978 Sep 19;42(3):265–279. doi: 10.1007/BF01870362. [DOI] [PubMed] [Google Scholar]
  16. Klebba P. E., McIntosh M. A., Neilands J. B. Kinetics of biosynthesis of iron-regulated membrane proteins in Escherichia coli. J Bacteriol. 1982 Mar;149(3):880–888. doi: 10.1128/jb.149.3.880-888.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Konisky J. Colicins and other bacteriocins with established modes of action. Annu Rev Microbiol. 1982;36:125–144. doi: 10.1146/annurev.mi.36.100182.001013. [DOI] [PubMed] [Google Scholar]
  18. Konisky J., Soucek S., Frick K., Davies J. K., Hammond C. Relationship between the transport of iron and the amount of specific colicin Ia membrane receptors in Escherichia coli. J Bacteriol. 1976 Jul;127(1):249–257. doi: 10.1128/jb.127.1.249-257.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Lipman D. J., Pearson W. R. Rapid and sensitive protein similarity searches. Science. 1985 Mar 22;227(4693):1435–1441. doi: 10.1126/science.2983426. [DOI] [PubMed] [Google Scholar]
  21. Lundrigan M. D., Kadner R. J. Nucleotide sequence of the gene for the ferrienterochelin receptor FepA in Escherichia coli. Homology among outer membrane receptors that interact with TonB. J Biol Chem. 1986 Aug 15;261(23):10797–10801. [PubMed] [Google Scholar]
  22. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  23. Mizuno T., Chou M. Y., Inouye M. A comparative study on the genes for three porins of the Escherichia coli outer membrane. DNA sequence of the osmoregulated ompC gene. J Biol Chem. 1983 Jun 10;258(11):6932–6940. [PubMed] [Google Scholar]
  24. Needleman S. B., Wunsch C. D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol. 1970 Mar;48(3):443–453. doi: 10.1016/0022-2836(70)90057-4. [DOI] [PubMed] [Google Scholar]
  25. Nikaido H., Vaara M. Molecular basis of bacterial outer membrane permeability. Microbiol Rev. 1985 Mar;49(1):1–32. doi: 10.1128/mr.49.1.1-32.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nikaido H., Wu H. C. Amino acid sequence homology among the major outer membrane proteins of Escherichia coli. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1048–1052. doi: 10.1073/pnas.81.4.1048. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Overbeeke N., Bergmans H., van Mansfeld F., Lugtenberg B. Complete nucleotide sequence of phoE, the structural gene for the phosphate limitation inducible outer membrane pore protein of Escherichia coli K12. J Mol Biol. 1983 Feb 5;163(4):513–532. doi: 10.1016/0022-2836(83)90110-9. [DOI] [PubMed] [Google Scholar]
  28. Payne S. M., Niesel D. W., Peixotto S. S., Lawlor K. M. Expression of hydroxamate and phenolate siderophores by Shigella flexneri. J Bacteriol. 1983 Sep;155(3):949–955. doi: 10.1128/jb.155.3.949-955.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Richardson J. S. The anatomy and taxonomy of protein structure. Adv Protein Chem. 1981;34:167–339. doi: 10.1016/s0065-3233(08)60520-3. [DOI] [PubMed] [Google Scholar]
  30. Robson B., Suzuki E. Conformational properties of amino acid residues in globular proteins. J Mol Biol. 1976 Nov 5;107(3):327–356. doi: 10.1016/s0022-2836(76)80008-3. [DOI] [PubMed] [Google Scholar]
  31. Rosenbusch J. P. Characterization of the major envelope protein from Escherichia coli. Regular arrangement on the peptidoglycan and unusual dodecyl sulfate binding. J Biol Chem. 1974 Dec 25;249(24):8019–8029. [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. Soucek S., Konisky J. Normal iron-enterochelin uptake in mutants lacking the colicin I outer membrane receptor protein of Escherichia coli. J Bacteriol. 1977 Jun;130(3):1399–1401. doi: 10.1128/jb.130.3.1399-1401.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tinoco I., Jr, Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973 Nov 14;246(150):40–41. doi: 10.1038/newbio246040a0. [DOI] [PubMed] [Google Scholar]

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