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. 1990 Jun;172(6):3450–3461. doi: 10.1128/jb.172.6.3450-3461.1990

Trehalose transport and metabolism in Escherichia coli.

W Boos 1, U Ehmann 1, H Forkl 1, W Klein 1, M Rimmele 1, P Postma 1
PMCID: PMC209157  PMID: 2160944

Abstract

Trehalose metabolism in Escherichia coli is complicated by the fact that cells grown at high osmolarity synthesize internal trehalose as an osmoprotectant, independent of the carbon source, although trehalose can serve as a carbon source at both high and low osmolarity. The elucidation of the pathway of trehalose metabolism was facilitated by the isolation of mutants defective in the genes encoding transport proteins and degradative enzymes. The analysis of the phenotypes of these mutants and of the reactions catalyzed by the enzymes in vitro allowed the formulation of the degradative pathway at low osmolarity. Thus, trehalose utilization begins with phosphotransferase (IITre/IIIGlc)-mediated uptake delivering trehalose-6-phosphate to the cytoplasm. It continues with hydrolysis to trehalose and proceeds by splitting trehalose, releasing one glucose residue with the simultaneous transfer of the other to a polysaccharide acceptor. The enzyme catalyzing this reaction was named amylotrehalase. Amylotrehalase and EIITre were induced by trehalose in the medium but not at high osmolarity. treC and treB encoding these two enzymes mapped at 96.5 min on the E. coli linkage map but were not located in the same operon. Use of a mutation in trehalose-6-phosphate phosphatase allowed demonstration of the phosphoenolpyruvate- and IITre-dependent in vitro phosphorylation of trehalose. The phenotype of this mutant indicated that trehalose-6-phosphate is the effective in vivo inducer of the system.

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Selected References

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  1. Blazy B., Ullmann A. Properties of cyclic AMP-independent catabolite gene activator proteins of Escherichia coli. J Biol Chem. 1986 Sep 5;261(25):11645–11649. [PubMed] [Google Scholar]
  2. 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]
  3. Brand B., Boos W. Convenient preparative synthesis of [14C]trehalose from [14C]glucose by intact Escherichia coli cells. Appl Environ Microbiol. 1989 Sep;55(9):2414–2415. doi: 10.1128/aem.55.9.2414-2415.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bremer E., Silhavy T. J., Weinstock G. M. Transposition of lambda placMu is mediated by the A protein altered at its carboxy-terminal end. Gene. 1988 Nov 15;71(1):177–186. doi: 10.1016/0378-1119(88)90089-3. [DOI] [PubMed] [Google Scholar]
  5. Brickman E., Soll L., Beckwith J. Genetic characterization of mutations which affect catabolite-sensitive operons in Escherichia coli, including deletions of the gene for adenyl cyclase. J Bacteriol. 1973 Nov;116(2):582–587. doi: 10.1128/jb.116.2.582-587.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Casadaban M. J. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol. 1976 Jul 5;104(3):541–555. doi: 10.1016/0022-2836(76)90119-4. [DOI] [PubMed] [Google Scholar]
  7. Csonka L. N. Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev. 1989 Mar;53(1):121–147. doi: 10.1128/mr.53.1.121-147.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Curtis S. J., Epstein W. Phosphorylation of D-glucose in Escherichia coli mutants defective in glucosephosphotransferase, mannosephosphotransferase, and glucokinase. J Bacteriol. 1975 Jun;122(3):1189–1199. doi: 10.1128/jb.122.3.1189-1199.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dinnbier U., Limpinsel E., Schmid R., Bakker E. P. Transient accumulation of potassium glutamate and its replacement by trehalose during adaptation of growing cells of Escherichia coli K-12 to elevated sodium chloride concentrations. Arch Microbiol. 1988;150(4):348–357. doi: 10.1007/BF00408306. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. Kleckner N., Roth J., Botstein D. Genetic engineering in vivo using translocatable drug-resistance elements. New methods in bacterial genetics. J Mol Biol. 1977 Oct 15;116(1):125–159. doi: 10.1016/0022-2836(77)90123-1. [DOI] [PubMed] [Google Scholar]
  13. Larsen P. I., Sydnes L. K., Landfald B., Strøm A. R. Osmoregulation in Escherichia coli by accumulation of organic osmolytes: betaines, glutamic acid, and trehalose. Arch Microbiol. 1987 Feb;147(1):1–7. doi: 10.1007/BF00492896. [DOI] [PubMed] [Google Scholar]
  14. Lengeler J. W., Mayer R. J., Schmid K. Phosphoenolpyruvate-dependent phosphotransferase system enzyme III and plasmid-encoded sucrose transport in Escherichia coli K-12. J Bacteriol. 1982 Jul;151(1):468–471. doi: 10.1128/jb.151.1.468-471.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. MACDONALD D. L., WONG R. Y. A CHEMICAL SYNTHESIS OF TREHALOSE 6-PHOSPHATE. Biochim Biophys Acta. 1964 May 11;86:390–392. doi: 10.1016/0304-4165(64)90066-2. [DOI] [PubMed] [Google Scholar]
  16. Maloy S. R., Nunn W. D. Selection for loss of tetracycline resistance by Escherichia coli. J Bacteriol. 1981 Feb;145(2):1110–1111. doi: 10.1128/jb.145.2.1110-1111.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Maréchal L. R. Transport and metabolism of trehalose in Escherichia coli and Salmonella typhimurium. Arch Microbiol. 1984 Jan;137(1):70–73. doi: 10.1007/BF00425810. [DOI] [PubMed] [Google Scholar]
  18. Postma P. W., Keizer H. G., Koolwijk P. Transport of trehalose in Salmonella typhimurium. J Bacteriol. 1986 Dec;168(3):1107–1111. doi: 10.1128/jb.168.3.1107-1111.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Sabourin D., Beckwith J. Deletion of the Escherichia coli crp gene. J Bacteriol. 1975 Apr;122(1):338–340. doi: 10.1128/jb.122.1.338-340.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Schmid K., Schupfner M., Schmitt R. Plasmid-mediated uptake and metabolism of sucrose by Escherichia coli K-12. J Bacteriol. 1982 Jul;151(1):68–76. doi: 10.1128/jb.151.1.68-76.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Scholte B. J., Schuitema A. R., Postma P. W. Characterization of factor IIIGLc in catabolite repression-resistant (crr) mutants of Salmonella typhimurium. J Bacteriol. 1982 Feb;149(2):576–586. doi: 10.1128/jb.149.2.576-586.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Singer M., Baker T. A., Schnitzler G., Deischel S. M., Goel M., Dove W., Jaacks K. J., Grossman A. D., Erickson J. W., Gross C. A. A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli. Microbiol Rev. 1989 Mar;53(1):1–24. doi: 10.1128/mr.53.1.1-24.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. St Pierre M. L. Isolation and mapping of Salmonella typhimurium mutants defective in the utilization of trehalose. J Bacteriol. 1968 Mar;95(3):1185–1186. doi: 10.1128/jb.95.3.1185-1186.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Yarmolinsky M. B., Wiesmeyer H., Kalckar H. M., Jordan E. HEREDITARY DEFECTS IN GALACTOSE METABOLISM IN ESCHERICHIA COLI MUTANTS, II. GALACTOSE-INDUCED SENSITIVITY. Proc Natl Acad Sci U S A. 1959 Dec;45(12):1786–1791. doi: 10.1073/pnas.45.12.1786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. de Lares L. B., Ratouchniak J., Casse F. Chromosomal location of gene governing the trehalose utilization in Escherichia coli K12. Mol Gen Genet. 1977 Mar 28;152(1):105–108. doi: 10.1007/BF00264946. [DOI] [PubMed] [Google Scholar]

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