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Pores in the outer membrane of Escherichia coli K12

Involvement of proteins b and e in the functioning of pores for nucleotides

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Summary

Mutants lacking outer membrane proteins were studied in order to investigate the role of these proteins in the functioning of aqueous pores through the outer membrane. Protein b is involved in the functioning of pores through which low concentrations of adenosine-monophosphate (AMP), guanosine-monophosphate (GMP), bis(paranitrophenyl)-phosphate (bis-PNPP) and, although less pronounced, also cytidine-monophosphate (CMP) enter the cell. In the absence of the receptor protein of phage T6, which facilitates the permeation of various nucleosides (Hantke, 1976), protein b plays a major role in the uptake of adenosine. Proteins c and d and the receptor proteins of phages lambda and T6 do not have a pore function for AMP, GMP, CMP and bis-PNPP. However, a newly discovered peptidoglycan-associated protein, protein e, can also mediate the permeation of the latter four components, but not of adenosine, through the outer membrane.

Protein b does not play a major role in the uptake of higher concentrations of AMP. Obviously mainly other pores are used under those conditions. The results strongly suggest that at low concentrations of nucleoside monophosphates (and possibly of other nutrients) protein b functions as a specific pore.

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References

  • Alphen, W. van, Lugtenberg, B., Berendsen, W.: Heptose-deficient mutants of Escherichia coli K12 deficient in up to three major outer membrane proteins. Molec. gen. Genet. 147, 263–269 (1976)

    PubMed  Google Scholar 

  • Alphen, W. van, Lugtenberg, B.: Influence of osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli. J. Bact. 131, 623–630 (1977)

    PubMed  Google Scholar 

  • Ames, B.N., Dubin, D.T.: The role of polyamines in the neutralization of bacteriophage deoxyribonucleic acid. J. biol. Chem. 235, 769–775 (1960)

    PubMed  Google Scholar 

  • Beacham, I.R., Kahana, R., Levy, L., Yagil, E.: Mutants of Escherichia coli K12 “cryptic”, or deficient in 5′-nucleotidase (uridine diphosphate-sugar hydrolase) and 3′-nucleotidase (cyclic phosphodiesterase) activity. J. Bact. 116, 957–964 (1973)

    PubMed  Google Scholar 

  • Beacham, I.R., Haas, D., Yagil, E.: Mutants of Escherichia coli “cryptic” for certain periplasmic enzymes: evidence for an alteration of the outer membrane. J. Bact. 129, 1034–1044 (1977)

    PubMed  Google Scholar 

  • Bradbeer, C., Woodrow, M.L., Khalifah, L.I.: Transport of vitamin B12 in Escherichia coli: common receptor system for vitamin B12 and bacteriophage BF23 on the outer membrane of the cell envelope. J. Bact. 125, 1032–1039 (1976)

    PubMed  Google Scholar 

  • Braun, V., Hancock, R.E.W., Hantke, K., Hartmann, A.: Functional organization of the outer membrane of Escherichia coli: phage and colicin receptors as components of iron uptake systems. J. Supramolec. Structure 5, 37–58 (1976)

    Google Scholar 

  • Brockman, R.W., Heppel, L.A.: On the localization of alkaline phosphatase and cyclic phosphodiesterase in Escherichia coli. Biochemistry 7, 2554–2561 (1968)

    PubMed  Google Scholar 

  • Chai, T., Foulds, J.: Demonstration of a missing outer membrane protein in tolG mutants of Escherichia coli. J. molec. Biol. 85, 465–474 (1974)

    Google Scholar 

  • Chai, T., Foulds, J.: Escherichia coli K12 tolF mutants: alterations in protein composition of the outer membrane. J. Bact. 130, 781–786 (1977)

    PubMed  Google Scholar 

  • Davies, J.K., Reeves, P.: Genetics of resistance to colicins in Escherichia coli K-12: cross resistance among colicins of group A. J. Bact. 123, 102–117 (1975)

    PubMed  Google Scholar 

  • Decad, G.M., Nikaido, H.: Outer membrane of gram-negative bacteria XII. Molecular-sieving function of cell wall. J. Bact. 128, 325–336 (1976)

    PubMed  Google Scholar 

  • Diedrich, D.L., Summers, A.O., Schnaitman, C.A.: Outer membrane proteins of Escherichia coli. V. Evidence that protein 1 and bacteriophage directed protein 2 are different polypeptides. J. Bact. 131, 598–607 (1977)

    PubMed  Google Scholar 

  • Di Girolamo, P.M., Bradbeer, C.: Transport of vitamin B12 in Escherichia coli. J. Bact. 106, 745–750 (1971)

    PubMed  Google Scholar 

  • Foulds, J.: tolF locus in Escherichia coli: chromosomal location and relationship to loci cm1B and tolD. J. Bact. 128, 604–608 (1976)

    PubMed  Google Scholar 

  • Hantke, K.: Phage T6-colicin K receptor and nucleoside transport in Escherichia coli. FEBS Lett. 70, 109–112 (1976)

    PubMed  Google Scholar 

  • Henning, U., Haller, I.: Mutants of Escherichia coli K12 lacking all ‘major’ proteins of the outer cell envelope membrane. FEBS Lett. 55, 161–164 (1975)

    PubMed  Google Scholar 

  • Henning, U., Schmidmayr, W., Hindennach, I.: Major proteins of the outer cell envelope membrane of Escherichia coli K-12: multiple species of protein I. Molec. gen. Genet. 154, 293–298 (1977)

    PubMed  Google Scholar 

  • Hindennach, I., Henning, U.: The major proteins of the Escherichia coli outer cell envelope membrane. Preparative isolation of all major membrane proteins. Europ. J. Biochem. 59, 207–213 (1975)

    PubMed  Google Scholar 

  • Ichihara, S., Mizushima, S.: Involvement of outer membrane proteins in enterochelin-mediated iron uptake in Escherichia coli. J. Biochem. (Japan) 81, 749–756 (1977)

    Google Scholar 

  • Lugtenberg, B., Bronstein, H., van Selm, N., Peters, R.: Peptido-glycanassociated outer membrane proteins in gramnegative bacteria. Biochim. biophys. Acta (Amst.) 465, 571–578 (1977)

    Google Scholar 

  • Lugtenberg, B., Meijers, J., Peters, R., van der Hoek, P., van Alphen, L.: Electrophoretic resolution of the ‘major outer membrane protein’ of Escherichia coli K12 into four bands. FEBS Lett. 58, 254–258 (1975)

    Article  PubMed  Google Scholar 

  • Lugtenberg, B., Peters, R., Bernheimer, H., Berendsen, W.: Influence of cultural conditions and mutations on the composition of the outer membrane proteins of Escherichia coli. Molec. gen. Genet. 147, 251–262 (1976)

    PubMed  Google Scholar 

  • Lutkenhaus, J.F.: Role of a major outer membrane protein in Escherichia coli. J. Bact. 131, 631–637 (1977)

    PubMed  Google Scholar 

  • Manning, P.A., Reeves, P.: Outer membrane of Escherichia coli K-12: tsx mutants (resistant to bacteriophage T6 and colicin K) lack an outer membrane protein Biochem. biophys. Res. Commun. 71, 466–471 (1976)

    PubMed  Google Scholar 

  • Nakae, T.: Outer membrane of Salmonella typhimurium. Reconstitution of sucrose-permeable membrane vesicles. Biochem. biophys. Res. Commun. 64, 1224–1230 (1975)

    PubMed  Google Scholar 

  • Nakae, T.: Outer membrane of Salmonella. Isolation of protein complex that produces transmembrane channels. J. biol. Chem. 251, 2176–2178 (1976a)

    PubMed  Google Scholar 

  • Nakae, T.: Identification of the outer membrane of E. coli that produces transmembrane channels in reconstituted vesicle membranes. Biochem. biophys. Res. Commun. 71, 877–884 (1976b)

    PubMed  Google Scholar 

  • Neu, H.C.: The 5′-nucleotidase of Escherichia coli. I. Purification and properties. J. biol. Chem. 242, 3896–3904 (1967a)

    PubMed  Google Scholar 

  • Neu, H.C.: The 5′-nucleotidase of Escherichia coli. II. Surface localization and purification of the Escherichia coli 5′-nucleotidase inhibitor. J. biol. Chem. 242, 3905–3911 (1967b)

    PubMed  Google Scholar 

  • Nikaido, H.: Outer membrane of Salmonella typhimurium. Transmembrane diffusion of some hydrophobic substances. Biochim. biophys. Acta (Amst.) 433, 118–132 (1976)

    Google Scholar 

  • Nossal, N.G., Heppel, L.A.: The release of enzymes by osmotic shock from Escherichia coli in exponential phase. J. biol. Chem. 241, 3055–3062 (1966)

    PubMed  Google Scholar 

  • Osborn, M.J., Gander, J.E., Parisi, E., Carson, J.: Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membrane. J. biol. Chem. 247, 3962–3972 (1972)

    PubMed  Google Scholar 

  • Pugsley, A.P., Reeves, P.: Iron uptake in colicin B-resistant mutants of Escherichia coli K-12. J. Bact. 126, 1052–1062 (1976a)

    PubMed  Google Scholar 

  • Pugsley, A.P., Reeves, P.: Characterization of group B colicin-resistant mutants of Escherichia coli K-12: colicin resistance and the role of enterochelin. J. Bact. 127, 218–228 (1976b)

    PubMed  Google Scholar 

  • Pugsley, A.P., Reeves, P.: Increased production of the outer membrane receptors for colieins B, D and M by Escherichia coli under iron starvation. Biochem. biophys. Res. Commun. 70, 846–853 (1976c)

    PubMed  Google Scholar 

  • Pugsley, A.P., Reeves, P.: The role of colicin receptors in the uptake of ferrienterochelin by Escherichia coli K-12. Biochem. biophys. Res. Commun. 74, 903–911 (1977)

    PubMed  Google Scholar 

  • Randall-Hazelbauer, L., Schwartz, M.: Isolation of the bacteriophage lambda receptor from Escherichia coli. J. Bact. 116, 1436–1446 (1973)

    PubMed  Google Scholar 

  • Rosenbusch, J.P.: Characterization of the major envelope protein from Escherichia coli. Regular arrangement on the peptidoglycan and unusual dodecyl sulphate binding. J. biol. Chem. 249, 8019–8029 (1974)

    PubMed  Google Scholar 

  • Sabet, S.F., Schnaitman, C.A.: Purification and properties of the colicin E3 receptor of Escherichia coli. J. biol. Chem. 248, 1797–1806 (1973)

    PubMed  Google Scholar 

  • Schmitges, C.J., Henning, U.: The major proteins of the Escherichia coli outer cell-envelope membrane. Heterogeneity of protein I. Europ. J. Biochem. 63, 47–52 (1976)

    PubMed  Google Scholar 

  • Schnaitman, C.A.: Protein composition of the cell wall and cytoplasmic membrane of Escherichia coli. J. Bact. 104, 890–901 (1970)

    PubMed  Google Scholar 

  • Schnaitman, C.A.: Outer membrane proteins of Escherichia coli. IV. Differences in outer membrane proteins due to strain and cultural differences. J. Bact. 118, 454–464 (1974)

    PubMed  Google Scholar 

  • Schweizer, M., Schwarz, H., Sonntag, I., Henning, U.: Mutational change of membrane architecture. Mutants of Escherichia coli K12 missing major proteins of the outer cell envelope membrane. Biochim. biophys. Acta (Amst.) 448, 474–491 (1976)

    Google Scholar 

  • Skurray, R.A., Hancock, R.E.W., Reeves, P.: Con- mutants: class of mutants in Escherichia coli K-12 lacking a major cell wall protein and defective in conjugation and adsorption of a bacteriophage. J. Bact. 119, 726–735 (1974)

    PubMed  Google Scholar 

  • Szmelcman, S., Hofnung, M.: Maltose transport in Escherichia coli K-12: involvement of the bacteriophage lambda receptor. J. Bact. 124, 112–118 (1975)

    PubMed  Google Scholar 

  • Verhoef, C., de Graaff, P.J., Lugtenberg, E.J.J.: Mapping of a gene for a major outer membrane protein of Escherichia coli K12 with the aid of a newly isolated bacteriophage. Molec. gen. Genet. 150, 103–105 (1977)

    PubMed  Google Scholar 

  • White, J.C., Di Girolamo, P.M., Fu, M.L., Preston, Y.A., Bradbeer, C.: Transport of vitamin B12 in Escherichia coli: location and properties of the initial B12-binding site. J. biol. Chem. 248, 3978–3986 (1973)

    PubMed  Google Scholar 

  • Yu, F., Mizushima, S.: Stimulation by lipopolysaccharide of the binding of outer membrane proteins 0–8 and 0–9 to the peptidoglycan layer of Escherichia coli K-12. Biochem. biophys. Res. Commun. 74, 1397–1402 (1977)

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Molecular Cell Biology, Section Microbiology, State University, Transitorium 3, Padualaan 8, Utrecht, The Netherlands

    Wim van Alphen, Nelke van Selm & Ben Lugtenberg

  2. Institute for Molecular Biology, State University, Transitorium 3, Padualaan 8, Utrecht, The Netherlands

    Wim van Alphen, Nelke van Selm & Ben Lugtenberg

Authors
  1. Wim van Alphen
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  2. Nelke van Selm
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  3. Ben Lugtenberg
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Communicated by H.G. Wittmann

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van Alphen, W., van Selm, N. & Lugtenberg, B. Pores in the outer membrane of Escherichia coli K12. Molec. Gen. Genet. 159, 75–83 (1978). https://doi.org/10.1007/BF00401750

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  • DOI: https://doi.org/10.1007/BF00401750

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