Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1993 Mar;175(6):1682–1686. doi: 10.1128/jb.175.6.1682-1686.1993

Induction of the lambda receptor is essential for effective uptake of trehalose in Escherichia coli.

W Klein 1, W Boos 1
PMCID: PMC203962  PMID: 8449875

Abstract

Trehalose transport in Escherichia coli after growth at low osmolarity is mediated by enzyme IITre of the phosphotransferase system (W. Boos, U. Ehmann, H. Forkl, W. Klein, M. Rimmele, and P. Postma, J. Bacteriol. 172:3450-3461, 1990). The apparent Km (16 microM) of trehalose uptake is low. Since trehalose is a good source of carbon and the apparent affinity of the uptake system is high, it was surprising that the disaccharide trehalose [O-alpha-D-glucosyl(1-1)-alpha-D-glucoside] has no problems diffusing through the outer membrane at high enough rates to allow full growth, particularly at low substrate concentrations. Here we show that induction of the maltose regulon is required for efficient utilization of trehalose. malT mutants that lack expression of all maltose genes, as well as lamB mutants that lack only the lambda receptor (maltoporin), still grow on trehalose at the usual high (10 mM) trehalose concentrations in agar plates, but they exhibit the half-maximal rate of trehalose uptake at concentrations that are 50-fold higher than in the wild-type (malT+) strain. The maltose system is induced by trehalose to about 30% of the fully induced level reached when grown in the presence of maltose in a malT+ strain or when grown on glycerol in a maltose-constitutive strain [malT(Con)]. The 30% level of maximal expression is sufficient for maximal trehalose utilization, since there is no difference in the concentration of trehalose required for the half-maximal rate of uptake in trehalose-grown strains with the wild-type gene (malT+) or with strains constitutive for the maltose system [malT(Con)]. In contrast, when the expression of the lambda receptor is reduced to less than 20% of the maximal level, trehalose uptake becomes less efficient. Induction of the maltose system by trehalose requires metabolism of trehalose. Mutants lacking amylotrehalase, the key enzyme in trehalose utilization, accumulate trehalose but do not induce the maltose system.

Full text

PDF
1682

Selected References

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

  1. Benz R., Francis G., Nakae T., Ferenci T. Investigation of the selectivity of maltoporin channels using mutant LamB proteins: mutations changing the maltodextrin binding site. Biochim Biophys Acta. 1992 Mar 2;1104(2):299–307. doi: 10.1016/0005-2736(92)90044-m. [DOI] [PubMed] [Google Scholar]
  2. Benz R., Schmid A., Nakae T., Vos-Scheperkeuter G. H. Pore formation by LamB of Escherichia coli in lipid bilayer membranes. J Bacteriol. 1986 Mar;165(3):978–986. doi: 10.1128/jb.165.3.978-986.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bochner B. R., Huang H. C., Schieven G. L., Ames B. N. Positive selection for loss of tetracycline resistance. J Bacteriol. 1980 Aug;143(2):926–933. doi: 10.1128/jb.143.2.926-933.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boos W., Ehmann U., Bremer E., Middendorf A., Postma P. Trehalase of Escherichia coli. Mapping and cloning of its structural gene and identification of the enzyme as a periplasmic protein induced under high osmolarity growth conditions. J Biol Chem. 1987 Sep 25;262(27):13212–13218. [PubMed] [Google Scholar]
  5. Boos W., Ehmann U., Forkl H., Klein W., Rimmele M., Postma P. Trehalose transport and metabolism in Escherichia coli. J Bacteriol. 1990 Jun;172(6):3450–3461. doi: 10.1128/jb.172.6.3450-3461.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brass J. M., Bauer K., Ehmann U., Boos W. Maltose-binding protein does not modulate the activity of maltoporin as a general porin in Escherichia coli. J Bacteriol. 1985 Feb;161(2):720–726. doi: 10.1128/jb.161.2.720-726.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Brass J. M., Manson M. D., Larson T. J. Transposon Tn10-dependent expression of the lamB gene in Escherichia coli. J Bacteriol. 1984 Jul;159(1):93–99. doi: 10.1128/jb.159.1.93-99.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bukau B., Ehrmann M., Boos W. Osmoregulation of the maltose regulon in Escherichia coli. J Bacteriol. 1986 Jun;166(3):884–891. doi: 10.1128/jb.166.3.884-891.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Davidson A. L., Nikaido H. Overproduction, solubilization, and reconstitution of the maltose transport system from Escherichia coli. J Biol Chem. 1990 Mar 15;265(8):4254–4260. [PubMed] [Google Scholar]
  10. Ehrmann M., Boos W. Identification of endogenous inducers of the mal regulon in Escherichia coli. J Bacteriol. 1987 Aug;169(8):3539–3545. doi: 10.1128/jb.169.8.3539-3545.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ferenci T., Muir M., Lee K. S., Maris D. Substrate specificity of the Escherichia coli maltodextrin transport system and its component proteins. Biochim Biophys Acta. 1986 Aug 7;860(1):44–50. doi: 10.1016/0005-2736(86)90496-7. [DOI] [PubMed] [Google Scholar]
  12. Ferenci T., Schwentorat M., Ullrich S., Vilmart J. Lambda receptor in the outer membrane of Escherichia coli as a binding protein for maltodextrins and starch polysaccharides. J Bacteriol. 1980 May;142(2):521–526. doi: 10.1128/jb.142.2.521-526.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Francoz E., Molla A., Dassa E., Saurin W., Hofnung M. The maltoporin of Salmonella typhimurium: sequence and folding model. Res Microbiol. 1990 Nov-Dec;141(9):1039–1059. doi: 10.1016/0923-2508(90)90078-5. [DOI] [PubMed] [Google Scholar]
  14. Freundlieb S., Ehmann U., Boos W. Facilitated diffusion of p-nitrophenyl-alpha-D-maltohexaoside through the outer membrane of Escherichia coli. Characterization of LamB as a specific and saturable channel for maltooligosaccharides. J Biol Chem. 1988 Jan 5;263(1):314–320. [PubMed] [Google Scholar]
  15. Giaever H. M., Styrvold O. B., Kaasen I., Strøm A. R. Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli. J Bacteriol. 1988 Jun;170(6):2841–2849. doi: 10.1128/jb.170.6.2841-2849.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gilson E., Rousset J. P., Charbit A., Perrin D., Hofnung M. malM, a new gene of the maltose regulon in Escherichia coli K12. I. malM is the last gene of the malK-lamB operon and encodes a periplasmic protein. J Mol Biol. 1986 Oct 5;191(3):303–311. doi: 10.1016/0022-2836(86)90127-0. [DOI] [PubMed] [Google Scholar]
  17. Gutierrez C., Ardourel M., Bremer E., Middendorf A., Boos W., Ehmann U. Analysis and DNA sequence of the osmoregulated treA gene encoding the periplasmic trehalase of Escherichia coli K12. Mol Gen Genet. 1989 Jun;217(2-3):347–354. doi: 10.1007/BF02464903. [DOI] [PubMed] [Google Scholar]
  18. Hengge-Aronis R., Klein W., Lange R., Rimmele M., Boos W. Trehalose synthesis genes are controlled by the putative sigma factor encoded by rpoS and are involved in stationary-phase thermotolerance in Escherichia coli. J Bacteriol. 1991 Dec;173(24):7918–7924. doi: 10.1128/jb.173.24.7918-7924.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hengge R., Boos W. Maltose and lactose transport in Escherichia coli. Examples of two different types of concentrative transport systems. Biochim Biophys Acta. 1983 Aug 11;737(3-4):443–478. doi: 10.1016/0304-4157(83)90009-6. [DOI] [PubMed] [Google Scholar]
  20. Kaasen I., Falkenberg P., Styrvold O. B., Strøm A. R. Molecular cloning and physical mapping of the otsBA genes, which encode the osmoregulatory trehalose pathway of Escherichia coli: evidence that transcription is activated by katF (AppR) J Bacteriol. 1992 Feb;174(3):889–898. doi: 10.1128/jb.174.3.889-898.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kellermann O., Szmelcman S. Active transport of maltose in Escherichia coli K12. Involvement of a "periplasmic" maltose binding protein. Eur J Biochem. 1974 Aug 15;47(1):139–149. doi: 10.1111/j.1432-1033.1974.tb03677.x. [DOI] [PubMed] [Google Scholar]
  22. Klein W., Ehmann U., Boos W. The repression of trehalose transport and metabolism in Escherichia coli by high osmolarity is mediated by trehalose-6-phosphate phosphatase. Res Microbiol. 1991 May;142(4):359–371. doi: 10.1016/0923-2508(91)90105-j. [DOI] [PubMed] [Google Scholar]
  23. Kühnau S., Reyes M., Sievertsen A., Shuman H. A., Boos W. The activities of the Escherichia coli MalK protein in maltose transport, regulation, and inducer exclusion can be separated by mutations. J Bacteriol. 1991 Apr;173(7):2180–2186. doi: 10.1128/jb.173.7.2180-2186.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Palmer T. N., Ryman B. E., Whelan W. J. The action pattern of amylomaltase from Escherichia coli. Eur J Biochem. 1976 Oct 1;69(1):105–115. doi: 10.1111/j.1432-1033.1976.tb10863.x. [DOI] [PubMed] [Google Scholar]
  25. Raibaud O., Richet E. Maltotriose is the inducer of the maltose regulon of Escherichia coli. J Bacteriol. 1987 Jul;169(7):3059–3061. doi: 10.1128/jb.169.7.3059-3061.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Reidl J., Boos W. The malX malY operon of Escherichia coli encodes a novel enzyme II of the phosphotransferase system recognizing glucose and maltose and an enzyme abolishing the endogenous induction of the maltose system. J Bacteriol. 1991 Aug;173(15):4862–4876. doi: 10.1128/jb.173.15.4862-4876.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Reyes M., Shuman H. A. Overproduction of MalK protein prevents expression of the Escherichia coli mal regulon. J Bacteriol. 1988 Oct;170(10):4598–4602. doi: 10.1128/jb.170.10.4598-4602.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Richet E., Vidal-Ingigliardi D., Raibaud O. A new mechanism for coactivation of transcription initiation: repositioning of an activator triggered by the binding of a second activator. Cell. 1991 Sep 20;66(6):1185–1195. doi: 10.1016/0092-8674(91)90041-v. [DOI] [PubMed] [Google Scholar]
  29. Schmid K., Ebner R., Jahreis K., Lengeler J. W., Titgemeyer F. A sugar-specific porin, ScrY, is involved in sucrose uptake in enteric bacteria. Mol Microbiol. 1991 Apr;5(4):941–950. doi: 10.1111/j.1365-2958.1991.tb00769.x. [DOI] [PubMed] [Google Scholar]
  30. Schwartz M., Hofnung M. La maltodextrine phosphorylase d'Escherichia coli. Eur J Biochem. 1967 Sep;2(2):132–145. doi: 10.1111/j.1432-1033.1967.tb00117.x. [DOI] [PubMed] [Google Scholar]
  31. Schwartz M. Sur l'existence chez Escherichia coli K 12 d'une régulation commune à la biosynthèse des récepteurs du bactériophage et au métabolisme du maltose. Ann Inst Pasteur (Paris) 1967 Nov;113(5):685–704. [PubMed] [Google Scholar]
  32. Schülein K., Schmid K., Benzl R. The sugar-specific outer membrane channel ScrY contains functional characteristics of general diffusion pores and substrate-specific porins. Mol Microbiol. 1991 Sep;5(9):2233–2241. doi: 10.1111/j.1365-2958.1991.tb02153.x. [DOI] [PubMed] [Google Scholar]
  33. Silhavy T. J., Hartig-Beecken I., Boos W. Periplasmic protein related to the sn-glycerol-3-phosphate transport system of Escherichia coli. J Bacteriol. 1976 May;126(2):951–958. doi: 10.1128/jb.126.2.951-958.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Szmelcman S., Hofnung M. Maltose transport in Escherichia coli K-12: involvement of the bacteriophage lambda receptor. J Bacteriol. 1975 Oct;124(1):112–118. doi: 10.1128/jb.124.1.112-118.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Szmelcman S., Schwartz M., Silhavy T. J., Boos W. Maltose transport in Escherichia coli K12. A comparison of transport kinetics in wild-type and lambda-resistant mutants as measured by fluorescence quenching. Eur J Biochem. 1976 May 17;65(1):13–19. doi: 10.1111/j.1432-1033.1976.tb10383.x. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES