1887

Abstract

A clinical isolate of was demonstrated to transport [C]maltose with similar kinetics to enteric bacteria ( : 0.3μM; : 22 nmol min per 10 cells). The uptake of [C]maltose was completely inhibited in the presence of unlabelled maltose or maltodextrins, whereas other mono- and disaccharides, such as glucose, galactose, sucrose, lactose or melibiose, had no effect. A protein with an apparent molecular mass of 39 kDa (maltose-binding protein; MBP) was identified in osmotic-shock fluid of maltose-grown cells by SDS-gel electrophoresis, and was purified to homogeneity by either amylose affinity chromatography or ion-exchange chromatography. Equilibrium dialysis experiments revealed the ability of the purified protein to bind [C]maltose with high affinity ( = 1.6μM). Unlabelled maltose and maltodextrins competed for the binding site. In a reconstitution experiment, MBP poorly restored the transport activity of a binding-protein-deficient () mutant. N-terminal sequence analyses of the purified native protein and of peptides generated by cleavage with CNBr and subsequently separated by HPLC revealed about 56% identical amino acid residues, as compared to enterobacterial MBPs. We conclude that maltose is transported into via a binding-protein-dependent transport system.

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1994-04-01
2021-10-17
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References

  1. Ames G.F.-L. Bacterial periplasmic transport systems: structure, mechanism, and evolution. Annu Rev Biochem 1986; 55:397–425
    [Google Scholar]
  2. Ames G.F.-L., Mimura C.S., Shyamala V. Bacterial periplasmic permeases belong to a family of transport proteins operating from Escherichia coli to human: traffic ATPases. FEMS Microbiol Rev 1990; 75:429–446
    [Google Scholar]
  3. Bahl H., Burchhardt G., Wienecke A. Nucleotide sequence of two Clostridium thermosulfurogenes EMI genes homologous to Escherichia coli genes encoding integral membrane components of binding protein-dependent transport systems. FEMS Microbiol Lett 1991; 81:83–88
    [Google Scholar]
  4. Baumann P., Schubert R.H.W. Vibrionaceae. In Bergey's Manual of Systematic Bacteriology 1984 Edited by Krieg N.R., Holt J.G. Baltimore & London: Williams & Wilkins; 1 pp 516–517
    [Google Scholar]
  5. Brass J. Calcium-induced permeabilization of the outer membrane: a method for reconstitution of periplasmic binding protein-dependent transport systems in Escherichia coli and Salmonella typhimurium. Methods Envymol 1986; 125:289–302
    [Google Scholar]
  6. Brzostek K., Heleszko H., Hrebenda J. Maltoporins and maltose-binding proteins of Yersinia enterocolitica. J Gen Microbiol 1993; 139:195–201
    [Google Scholar]
  7. Chakraborty T., Montenegro M.A., Sanyal S.C., Helmuth R., Bulling E., Timmis K.N. Cloning of enterotoxin gene from Aeromonas hydrophila provides exclusive evidence of production of a cytotoxic enterotoxin. Infect Immun 1984; 46:435–441
    [Google Scholar]
  8. Chakraborty T., Huhle B., Hof H., Bergbauer H., Goebel W. Marker exchange mutagenesis of the aerolysin determinant in Aeromonas hydrophila demonstrates the role of aerolysin in A. hydrophila-associated systemic infections. Infect Immun 1987; 55:2274–2280
    [Google Scholar]
  9. Dahl M.K., Manson M.D. Interspecific reconstitution of maltose transport and chemotaxis in Escherichia coli with maltose-binding protein from various enteric bacteria. J Bacterial 1985; 164:1057–1063
    [Google Scholar]
  10. Dahl M.K., Francoz E., Saurin W., Boos W., Manson M.D., Hofnung M. Comparison of sequences from the malB regions of Salmonella typhimurium and Enterobacter aerogenes with Escherichia coli K12: a potential new regulatory site in the interoperonic region. Mol & Gen Genet 1989; 218:199–207
    [Google Scholar]
  11. Dassa E. Sequence-function relationships in MalG, an inner membrane protein from the maltose transport system in Escherichia coli. Mol Microbiol 1993; 7:39–47
    [Google Scholar]
  12. Davidson A.L., Nikaido H. Purification and characterization of the membrane-associated components of the maltose transport system from Escherichia coli. J Biol Chem 1991; 266:8946–8951
    [Google Scholar]
  13. Davidson A.L., Shuman H.A., Nikaido H. Mechanism of maltose transport in Escherichia coli: transmembrane signaling by periplasmic binding proteins. Proc Natl Acad Sci USA 1992; 89:2360–2364
    [Google Scholar]
  14. Dean D.A., Hor L.I., Shuman H.A., Nikaido H. Interaction between maltose-binding protein and the membrane-associated maltose transporter complex in Escherichia coli. Mol Microbiol 1992; 6:2033–2040
    [Google Scholar]
  15. Dulley J.R., Grieve P.A. A simple technique for eliminating interference by detergents in the Lowry method of protein determination. Anal Biochem 1975; 64:136–141
    [Google Scholar]
  16. Duplay P., Szmelcman S., Bedouelle H., Hofnung M. Silent and functional changes in the periplasmic maltose-binding protein of Escherichia coli K12. I. Transport of maltose. J Mol Biol 1987; 194:663–673
    [Google Scholar]
  17. Ferenci T., Klotz U. Affinity chromatographic isolation of the periplasmic maltose binding protein of Escherichia coli. FEBS Lett 1978; 94:213–217
    [Google Scholar]
  18. Gilson E., Alloing G., Schmidt T., Claverys J.-P., Dudler R., Hofnung M. Evidence for high affinity binding-protein dependent transport systems in Gram-positive bacteria and in Mycoplasma. EMBO 1988; 7:3971–3974
    [Google Scholar]
  19. Gobius K.I., Pemberton J.M. Molecular cloning, characterization, and nucleotide sequence of an extracellular amylase gene from Aeromonas hydrophila. J Bacteriol 1988; 170:325–1332
    [Google Scholar]
  20. Higgins C.F. ABC transporter: from microorganisms to man. Amu Rev Cell Biol 1992; 8:67–113
    [Google Scholar]
  21. Janda J.M. Biochemical and exoenzymatic properties of Aeromonas species. Diagn Microbiol Infect Dis 1985; 3:223–232
    [Google Scholar]
  22. Jeanteur D., Gletsu N., Pattus F., Buckley J.T. Purification of Aeromonas hydrophila major outer-membrane proteins: N-terminal sequence analysis and channel-forming properties. Mol Microbiol 1992; 6:3355–3363
    [Google Scholar]
  23. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680–685
    [Google Scholar]
  24. Leung K.Y., Stevenson R.M.W. Tn5-induced protease-deficient strains of Aeromonas hydrophila with reduced virulence for fish. Infect Immun 1988; 56:2639–2644
    [Google Scholar]
  25. Miller J.H. Experiments in Molecular Genetics 1972 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.;
    [Google Scholar]
  26. Nossal N.G., Heppel L.A. The release of enzymes by osmotic shock from Escherichia coli in exponential phase. J Biol Chem 1966; 241:3055–3062
    [Google Scholar]
  27. Ochman H., Wilson A.C. Evolutionary history of enteric bacteria. In Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology 1987 Edited by Ingraham J.L., Low K.B., Magasanik B., Umbarger H.E. Washington, DC: American Society for Microbiology; pp 1649–1654
    [Google Scholar]
  28. Puyet A., Espinosa M. Structure of the maltodextrin-uptake locus of Streptococcus pneumoniae Correlation to the Escherichia coli maltose regulon. J Mol Biol 1993; 230:800–811
    [Google Scholar]
  29. Roth J.R. Genetic techniques in studies of bacterial metabolism. Methods Enszymol 1970; 17:3–35
    [Google Scholar]
  30. Russell R.R.B., Aduse-Opoku J., Sutcliffe I.C., Tao L., Ferretti J.J. A binding protein-dependent transport system in Streptococcus mutans responsible for multiple sugar metabolism. J Biol Chem 1992; 267:4631–4637
    [Google Scholar]
  31. Schekjger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 1987; 166:368–379
    [Google Scholar]
  32. Schneider E. Periplasmic binding protein-dependent transport of maltose/maltodextrins in Escherichia coli and Salmonella typhimurium. In Trends in Biomembranes and Bioenergetics 1990 Edited by Jacob A. Trivandrum: India: Research Trends; 1 pp 201–218
    [Google Scholar]
  33. Schneider E., Francoz E., Dassa E. Completion of the nucleotide sequence of the ‘maltose B’ region in Salmonella typhimurium' the high conservation of the malM gene suggests a selected physiological role for its product. Biochim Biophys Acta 1992; 1129:223–227
    [Google Scholar]
  34. Schwartz M. The maltose regulon. In Escherichia coli and Salmonella typhimurium. Cellular and Molecular Biology 1987 Edited by Ingraham J.L., Low K.B., Magasanik B., Umbarger H.E. Washington, DC: American Society for Microbiology; 1 pp 1482–1502
    [Google Scholar]
  35. Shuman H.A. Active transport of maltose in Escherichia coli K12 Role of the periplasmic maltose-binding protein and evidence for a substrate recognition site in the cytoplasmic membrane. J Biol Chem 1982; 247:5455–5461
    [Google Scholar]
  36. Spurlino J.C., Lu G.-Y., Quiocho F.A. The 23-A resolution structure of the maltose- or maltodextrin-binding protein, a primary receptor of bacterial active transport and chemotaxis. J Biol Chem 1991; 266:5202–5219
    [Google Scholar]
  37. Tagney M., Smith P., Priest F.G., Mitchell W.J. Maltose uptake and its regulation in Bacillus subtilis. FEMS Microbiol Lett 1992a; 97:191–196
    [Google Scholar]
  38. Tagney M., Smith P., Priest F.G., Mitchell W.J. Maltose transport in Bacillus licheniformis NCIB 6346. J Gen Microbiol 1992b; 138:1821–1827
    [Google Scholar]
  39. Walker J.E., Saraste M., Runswick M.J., Gay N.J. Distantly related sequences in the a- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1982; 1:945–951
    [Google Scholar]
  40. Walter C., Httner zu Bentrup K., Schneider E. Large scale purification, nucleotide binding properties, and ATPase activity of the MalK subunit of Salmonella typhimurium maltose transport complex. J Biol Chem 1992; 267:8863–8869
    [Google Scholar]
  41. Woese C.R. Bacterial evolution. Microbiol Rep 1987; 51:221–271
    [Google Scholar]
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