Identification of TonB homologs in the family Enterobacteriaceae and evidence for conservation of TonB-dependent energy transduction complexes

Journal of Bacteriology

Volumn 178, Issue 5, 1996, Pages 1363-1373

  Larsen, Ray A ^a   Myers, Paul S ^a   Skare, Jonathan T ^a,c   Seachord, Carrie L ^b   Darveau, Richard P ^b   Postle, Kathleen ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b BRISTOL MYERS SQUIBB   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYANOCOBALAMIN; SIDEROPHORE;

ACTIVE TRANSPORT; ARTICLE; CITROBACTER; ENERGY TRANSFER; ENTEROBACTERIACEAE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEUS; SHIGELLA;

CITROBACTER; EDWARDSIELLA TARDA; ENTEROBACTERIACEAE; ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; KLUYVERA; MURINAE; NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS PUTIDA; SHIGELLA; YERSINIA ENTEROCOLITICA;

EID: 0029958770     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.178.5.1363-1373.1996     Document Type: Article

References (56)

1. Ahmad, S., W. G. Weisburg, and R. A. Jensen. 1990. Evolution of aromatic amino acid biosynthesis and application to the fine-tuned phylogenetic positioning of enteric bacteria. J. Bacteriol. 172:1051-1061.
2. Ahmer, B. M. M., M. G. Thomas, R. A. Larsen, and K. Postle. 1994. Characterization of the exbBD operon of Escherichia coli and the role of ExbB and ExbD in TonB function and stability. J. Bacteriol 177:4742-4747.
3. 12 in tonB mutants of Escherichia coli. J. Bacteriol. 128:242-247.
4. Bell, P. E., C. D. Nau, J. T. Brown, J. Konisky, and R. J. Kadner. 1990. Genetic suppression demonstrates interaction of TonB protein with outer membrane transport proteins in Escherichia coli. J. Bacteriol. 172:3826-3829.
5. Bitter, W., J. Tommassen, and P. J. Weisbeek. 1993. Identification and characterization of the exbB, exbD and tonB genes of Pseudomonas putida WCS358: their involvement in ferric-pseudobactin transport. Mol. Microbiol. 7:117-130.
6. Bradbeer, C. 1993 The proton motive force drives the outer membrane transport of cobalamin in Escherichia coli. J. Bacteriol. 175:3146-3150.
7. Bruske, A. K., M. Anton, and K. J. Heller. 1993. Cloning and sequencing of the Klebsiella pneumoniae tonB gene and characterization of hybrid proteins formed between Escherichia coli and K. pneumoniae TonB Gene 131:9-16.
8. Bruske, A. K., and K. J. Heller. 1993. Molecular characterization of the Enterobacter aerogenes tonB gene: identification of a novel type of TonB box suppressor mutant. J. Bacteriol. 175:6158-6168.
9. Byrd, T. F., and M. A. Horwitz. 1991. Chloroquine inhibits the intracellular multiplication of Legionella pneumophila by limiting the availability of iron: a potential new mechanism for the therapeutic effect of chloroquine against intracellular pathogens. J. Clin. Invest. 88:351-357.
10. Cornelissen, C. N., G. D. Biswas, J. Tsai, D. K. Paruchuri, S. A. Thompson, and P. F. Sparling. 1992 Gonococcal transferrin-binding protein 1 is required for transferrin utilization and is homologous to TonB-dependent outer membrane receptors J. Bacteriol. 174:5788-5797.
11. Devereux, J., P. Haeberli, and O. Smithies. 1985. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 13:387-395.
12. Eick-Helmerich, K., and V. Braun. 1989. Import of biopolymers into Escherichia coli: nucleotide sequences of the exbB and exbD genes are homologous to those of the tolQ and tolR genes, respectively. J. Bacteriol. 171:5117-5126.
13. Elkins, C., C.-J. Chen, and C. E. Thomas. 1995. Characterization of the hgbA locus encoding a hemoglobin receptor from Haemophilus ducreyi. Infect. Immun. 63:2194-2200.
14. Fortier, A. H., D. A. Leiby, R. B. Narayanan, E. Asafoadjei, R. M. Crawford, C. A. Nacy, and M. S. Meltzer. 1995. Growth of Francisella tularensis LVS in macrophages: the acidic intracellular compartment provides essential iron required for growth. Infect. Immun. 63:1478-1483.
15. Frost, G. E., and H. Rosenberg. 1975. Relationship between the tonB locus and iron transport in Escherichia coli J. Bacteriol. 124:704-712.
16. Gaisser, S., and V. Braun. 1991. The tonB gene of Serratia marcescens. sequence, activity and partial complementation of Escherichia coli tonB mutants. Mol. Microbiol. 5:2777-2787.
17. Goldberg, M. B., S. A. Boyko, J. R. Butterton, J. A. Stoebner, S. M. Payne, and S. B. Calderwood. 1992. Characterization of a Vibrio cholerae virulence factor homologous to the family of TonB-dependent proteins. Mol. Microbiol. 6:2407-2418.
18. Guterman, S. K., and L. Dann. 1973. Excretion of enterochelin by exbA and exbB mutants of Escherichia coli. J. Bacteriol. 114:1225-1230.
19. Hancock, R. E. W., and V. Braun. 1976. Nature of the energy requirement for the irreversible adsorption of bacteriophage T1 and φ80 to Escherichia coli. J. Bacteriol. 125:409-415.
20. Hannavy, K., G. C. Barr, C. J. Dorman, J. Adamson, L. R. Mazengera, M. P. Gallagher, J. S. Evans, B. A. Levine, I. P. Trayer, and C. F. Higgins. 1990. TonB protein of Salmonella typhimurium: a model for signal transduction between membranes J. Mol Biol. 216:897-910.
21. Hantke, K., and V. Braun. 1975. Membrane receptor dependent iron transport in Escherichia coli. FEBS Lett. 49:301-305.
22. 12 and ferric iron transport. FEMS Lett. 12:31-35.
23. Heller, K., R. J. Kadner, and K. Günter. 1988. 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 64:147-153.
24. Hill, C. W., and B. W. Harnish. 1981. Inversions between ribosomal RNA genes of Eschenchia coli. Proc Natl. Acad. Sci. USA 78:7069-7072
25. Jarosik, G. P., and E. J. Hansen. 1995. Cloning and sequencing of the Haemophilus influenzae exbB and exbD genes. Gene 152:89-92
26. Jarosik, G. P., J. D. Sanders, L. D. Cope, U. Muller-Eberhard, and E. J. Hansen. 1994. A functional tonB gene is required for both utilization of heme and virulence expression by Haemophilus influenzae type b. Infect. Immun. 62:2470-2477.
27. Jaskula, J. C., T. E. Letain, S. K. Roof, J. T. Skare, and K. Postle. 1994. Role of the TonB amino terminus in energy transduction between membranes. J. Bacteriol. 176:2326-2338.
28. Kampfenkel, K., and V. Braun. 1993. Membrane topologies of the TolQ and TolR proteins of Escherichia coli: inactivation of TolQ by a missense mutation in the proposed first transmembrane segment. J. Bacteriol. 175:4485-4491.
29. Klebba, P. E., J. M. Rutz, J. Liu, and C. K. Murphy. 1993. Mechanisms of TonB-catalyzed iron transport through the enteric bacterial cell envelope J. Bioenerg. Biomembr. 25:603-611.
30. Koebnik, R., A. J. Bäumler, J. Heesemann, V. Braun, and K. Hantke. 1993. The TonB protein of Yersinia enterocolitica and its interactions with TonB-box proteins. Mol. Gen. Genet. 237:152-160.
31. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydrophobic character of a protein. J Mol. Biol. 157:105-132.
32. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685
33. Larsen, R. A., and K. Postle. Unpublished observations.
34. Larsen, R. A., M. G. Thomas, G. E. Wood, and K. Postle. 1994. Partial suppression of an Eschenchia coli TonB transmembrane domain mutation (ΔV17) by a missense mutation in ExbB. Mol. Microbiol. 13:627-640
35. Larsen, R. A., G. E. Wood, and K. Postle. 1993. The conserved proline-rkh motif is not essential for energy transduction by Escherichia coli TonB protein. Mol. Microbiol 10:943-953.
36. Lundrigan, M. D., and R. J. Kadner. 1986. Nucleotide sequence of the ferrienterochelin receptor FepA in Escherichia coli: homology among outer membrane receptors that interact with TonB. J. Biol. Chem. 261:10797-10801.
37. Means, G. E., and R. E. Feeney. 1971. Chemical modifications of proteins. Holden-Day, Inc., San Francisco.
38. Nguyen, T. T. 1987. Ph D. thesis. University of California, Irvine.
39. Parks, Y. M., and G. V. Stauffer. 1989. DNA sequence of the metC gene and its flanking regions from Salmonella typhimurium LT2 and homology with the corresponding sequence of Eschenchia coli. Mol. Gen. Genet. 216:164-169.
40. Pettersson, A., P. van der Ley, J. T. Poolman, and J. Tommassen. 1993. Molecular characterization of the 98-kilodalton iron-regulated outer membrane protein of Neisseria meningitidis. Infect. Immun. 61:4724-4733
41. Postle, K. 1990. Aerobic regulation of the Eschenchia coli tonB gene by changes in iron availability and the fur locus. J. Bacteriol. 172:2287-2293.
42. Postle, K. 1993. TonB protein and energy transduction between membranes. J. Bioenerg. Biomembr. 25:591-601.
43. Postle, K., and R. F. Good. 1983. DNA sequence of the Escherichia coli tonB gene. Proc. Natl. Acad. Sci. USA 80:5235-5239.
44. Postle, K., and W. S. Reznikoff. 1979. Identification of the Escherichia coli tonB gene product in minicells containing tonB hybrid plasmids. J Mol Biol. 131:619-636.
45. Postle, K., and J. T. Skare. 1988 Escherichia coli TonB protein is exported from the cytoplasm without proteolytic cleavage of its amino terminus. J. Biol. Chem. 263:11000-11007.
46. 12 in Eschenchia coli. J. Biol. Chem. 255:4313-4319.
47. Roof, S. K., J. D. Allard, K. P. Bertrand, and K. Postle. 1991 Analysis of Escherichia coli TonB membrane topology by use of PhoA fusions J. Bacteriol. 173:5554-5557.
48. Ross, C., and K. Postle. Unpublished observations.
49. Rutz, J. M., T. Abdullah, S. P. Singh, V. I. Kalve, and P. E. Klebba. 1991. Evolution of the ferric enterobacting receptor in gram-negative bacteria. J. Bacteriol. 173:5964-5974.
50. Schöffler, H., and V. Braun. 1989. Transport across the outer membrane of Escherichia coli K12 via the FhuA receptor is regulated by the TonB protein of the cytoplasmic membrane. Mol Gen. Genet. 217:378-383.
51. Schramm, E., J. Mende, V. Braun, and R. M. Kamp. 1987. Nucleotide sequence of the colicin B activity gene cba: consensus pentapeptide among TonB-dependent colicins and receptors. J Bacteriol. 169:3350-3557.
52. Silhavy, T. J., M. L. Berman, and L. W. Enquist. 1984. Experiments with gene fusions. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
53. Skare, J. T. 1992. Ph.D. thesis. Washington State University, Pullman.
54. Skare, J. T., B. M. M. Ahmer, C. L. Seachord, R. P. Darveau, and K. Postle. 1993. Energy transduction between membranes: TonB, a cytoplasmic membrane protein, can be chemically cross-linked in vivo to the outer membrane receptor FepA. J. Biol. Chem. 268:16302-16308.
55. Skare, J. T., and K. Postle. 1991. Evidence for a TonB-dependent energy transduction complex in Escherichia coli. Mol. Microbiol 5:2883-2890.
56. Skare, J. T., S. K. Roof, and K. Postle. 1989. A mutation in the amino terminus of a hybrid TrpC-TonB protein relieves overproduction lethality and results in cytoplasmic accumulation. J. Bacteriol. 171:4442-4447.