DOI: 10.1128/jb.173.3.1187-1192.1991. Synthesis, accumulation, and excretion of trehalose in osmotically stressed Escherichia coli K-12 strains: influence of amber suppressors and function of the periplasmic trehalase

Synthesis, accumulation, and excretion of trehalose in osmotically stressed Escherichia coli K-12 strains: influence of amber suppressors and function of the periplasmic trehalase

10.1128/jb.173.3.1187-1192.1991

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

It has been reported previously that Escherichia coli K-12 carries an amber mutation that prevents osmotic stress-dependent accumulation of trehalose (M. L. Rod, K. Y. Alam, P. R. Cunningham, and D. P. Clark, J. Bacteriol. 170:3601-3610, 1988). We report that E. coli K-12 and W1485 (sup0) accumulated trehalose but that they required a higher osmotic strength in the growth medium than that required by their sup+ derivatives. Furthermore, the sup+ derivatives displayed both strongly increased trehalose-6-phosphate synthase activity and expression of otsA-lacZ and otsB-lacZ operon fusions compared with their parental strains. It is suggested that the amber mutation in question may be in a gene system encoding a transcriptional activator of the ots genes which govern the synthase. The much-used sup0 strain MC4100 behaved like the sup+ derivatives of W1485 with respect to trehalose synthesis. treA mutants with a defective periplasmic trehalase accumulated trehalose extracellularly under osmotic stress. The amount of trehalose excreted correlated with their synthase activity. Strains with an intact trehalase did not display extracellular trehalose accumulation. Thus, stressed E. coli cells regulate the cytoplasmic level of trehalose by a futile cycle involving overproduction, excretion, and degradation to glucose, which is reutilized.

Bibliography

Styrvold, O. B., & StrÃ¸m, A. R. (1991). Synthesis, accumulation, and excretion of trehalose in osmotically stressed Escherichia coli K-12 strains: influence of amber suppressors and function of the periplasmic trehalase. Journal of Bacteriology, 173(3), 1187â1192.

Authors 2

O B Styrvold (first)
A R Strøm (additional)

References 26 Referenced 82

Bakker , E. P. , I. R. Booth , U. Dinnbier , W. Epstein , and A. Gajewska . 1987 . Evidence for multiple K+ export systems in Escherichia coli . J. Bacteriol. 169 : 3743 - 3749 . (10.1128/jb.169.8.3743-3749.1987) / J. Bacteriol. / Evidence for multiple K+ export systems in Escherichia coli by Bakker E. P. (1987)
Becerra de Lares , L. , J. Ratouchniak , and F. Casse . 1977 . Chromosomal location of gene governing the trehalose utilization in Escherichia coli K12 . Mol. Gen. Genet. 152 : 105 - 108 . (10.1007/BF00264946) / Mol. Gen. Genet. / Chromosomal location of gene governing the trehalose utilization in Escherichia coli K12 by Becerra de Lares L. (1977)
Boos , W. , U. Ehmann , E. Bremer , A. Middendorf , and P. Postma . 1987 . 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. 262 : 13212 - 13218 . (10.1016/S0021-9258(18)45189-7) / J. Biol. Chem. / 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 by Boos W. (1987)
Boos , W. , U. Ehmann , H. Forkl , W. Klein , M. Rimmele , and P. Postma . 1990 . Trehalose transport and metabolism in Escherichia coli . J. Bacteriol. 172 : 3450 - 3461 . (10.1128/jb.172.6.3450-3461.1990) / J. Bacteriol. / Trehalose transport and metabolism in Escherichia coli by Boos W. (1990)
Bremer , E. , T. J. Silhavy , and G. M. Weinstock . 1985 . Transposable placMu bacteriophages for creating lacZ operon fusions and kanamycin resistance insertions in Escherichia coli . J. Bacteriol. 162 : 1092 - 1099 . (10.1128/jb.162.3.1092-1099.1985) / J. Bacteriol. / Transposable placMu bacteriophages for creating lacZ operon fusions and kanamycin resistance insertions in Escherichia coli by Bremer E. (1985)
Cairney , J. , I. R. Booth , and C. F. Higgins . 1985 . Osmoregulation of gene expression in Salmonella typhimurium: proU encodes an osmotically induced betaine transport system . J. Bacteriol. 164 : 1224 - 1232 . (10.1128/jb.164.3.1224-1232.1985) / J. Bacteriol. / Osmoregulation of gene expression in Salmonella typhimurium: proU encodes an osmotically induced betaine transport system by Cairney J. (1985)
Csonka , L. N. 1982 . A third L-proline permease in Salmonella typhimurium which functions in media of elevated osmotic strength . J. Bacteriol. 151 : 1433 - 1443 . (10.1128/jb.151.3.1433-1443.1982) / J. Bacteriol. / A third L-proline permease in Salmonella typhimurium which functions in media of elevated osmotic strength by Csonka L. N. (1982)
Csonka , L. N. 1989 . Physiological and genetic responses of bacteria to osmotic stress . Microbiol. Rev. 53 : 121 - 147 . (10.1128/mr.53.1.121-147.1989) / Microbiol. Rev. / Physiological and genetic responses of bacteria to osmotic stress by Csonka L. N. (1989)
Dinnbier , U. , E. Limpinsel , R. Schmid , and E. P. Bakker . 1988 . 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. 150 : 348 - 357 . (10.1007/BF00408306) / Arch. Microbiol. / 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 by Dinnbier U. (1988)
Epstein , W. 1986 . Osmoregulation by potassium transport in Escherichia coli . FEMS Microbiol. Rev. 39 : 73 - 78 . (10.1111/j.1574-6968.1986.tb01845.x) / FEMS Microbiol. Rev. / Osmoregulation by potassium transport in Escherichia coli by Epstein W. (1986)
Eshoo , M. W. 1989 . lac fusion analysis of the bet genes of Escherichia coli: regulation by osmolarity, temperature, oxygen, choline, and glycine betaine . J. Bacteriol. 170 : 5208 - 5215 . (10.1128/jb.170.11.5208-5215.1988) / J. Bacteriol. / lac fusion analysis of the bet genes of Escherichia coli: regulation by osmolarity, temperature, oxygen, choline, and glycine betaine by Eshoo M. W. (1989)
Giaever , H. M. , 0. B. Styrvold , I. Kaasen , and A. R. Str 0m. 1988 . Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli . J. Bacteriol. 170 : 2841 - 2849 . (10.1128/jb.170.6.2841-2849.1988) / J. Bacteriol. / Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli by Giaever H. M. (1988)
Gutierrez , C. , M. Ardourel , E. Bremer , A. Middendorf , W. Boos , and U. Ehmann . 1989 . Analysis and DNA sequence of the osmoregulated treA gene encoding the periplasmic trehalase of Escherichia coli K12 . Mol. Gen. Genet. 217 : 347 - 354 . (10.1007/BF02464903) / Mol. Gen. Genet. / Analysis and DNA sequence of the osmoregulated treA gene encoding the periplasmic trehalase of Escherichia coli K12 by Gutierrez C. (1989)
Herbert D. P. J. Phipps and R. E. Strange. 1971. Chemical analysis of microbial cells p. 209-344. In J. R. Norris and D. W. Ribbons (ed.) Methods in microbiology vol. SB. Academic Press Inc. (London) Ltd. London. (10.1016/S0580-9517(08)70641-X)
Herzog , R. M. , E. A. Galinski , and H. G. Trtuper . 1990 . Degradation of the compatible solute trehalose in Ectothiorhodospira halochloris: isolation and characterization of trehalase . Arch. Microbiol. 153 : 600 - 606 . (10.1007/BF00245272) / Arch. Microbiol. / Degradation of the compatible solute trehalose in Ectothiorhodospira halochloris: isolation and characterization of trehalase by Herzog R. M. (1990)
Kaasen I. P. Falkenberg 0. B. Styrvold and A. R. Str 0m. Unpublished results.
Landfald , B. , and A. R. Str 0m. 1986 . Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli . J. Bacteriol. 165 : 849 - 855 . (10.1128/jb.165.3.849-855.1986) / J. Bacteriol. / Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli by Landfald B. (1986)
Larsen , P. I. , L. K. Sydnes , B. Landfald , and A. R. Str 0m. 1987 . Osmoregulation in Escherichia coli by accumulation of organic osmolytes: betaines, glutamic acid, and trehalose . Arch. Microbiol. 147 : 1 - 7 . (10.1007/BF00492896) / Arch. Microbiol. / Osmoregulation in Escherichia coli by accumulation of organic osmolytes: betaines, glutamic acid, and trehalose by Larsen P. I. (1987)
Le Rudulier , D. , A. R. Str 0m, A. M. Dandekar , L. T. Smith , and R. C. Valentine . 1984 . Molecular biology of osmoregulation . Science 224 : 1064 - 1068 . (10.1126/science.224.4653.1064) / Science / Molecular biology of osmoregulation by Le Rudulier D. (1984)
Marechal , L. R. 1984 . Transport and metabolism of trehalose in Escherichia coli and Salmonella typhimurium . Arch. Microbiol. 137 : 70 - 73 . (10.1007/BF00425810) / Arch. Microbiol. / Transport and metabolism of trehalose in Escherichia coli and Salmonella typhimurium by Marechal L. R. (1984)
Miller J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
Perroud , B. , and D. Le Rudulier . 1985 . Glycine betaine transport in Escherichia coli: osmotic modulation . J. Bacteriol. 161 : 393 - 401 . (10.1128/jb.161.1.393-401.1985) / J. Bacteriol. / Glycine betaine transport in Escherichia coli: osmotic modulation by Perroud B. (1985)
Rod , M. L. , K. Y. Alam , P. R. Cunningham , and D. P. Clark . 1988 . Accumulation of trehalose by Escherichia coli K-12 at high osmotic pressure depends on the presence of amber suppressors . J. Bacteriol. 170 : 3601 - 3610 . (10.1128/jb.170.8.3601-3610.1988) / J. Bacteriol. / Accumulation of trehalose by Escherichia coli K-12 at high osmotic pressure depends on the presence of amber suppressors by Rod M. L. (1988)
Schweizer , H. , and W. Boos . 1983 . Transfer of the A(argFlac)U169 mutation between Escherichia coli strains by selection for a closely linked TnlO insertion . Mol. Gen. Genet. 192 : 293 - 294 . (10.1007/BF00327683) / Mol. Gen. Genet. / Transfer of the A(argFlac)U169 mutation between Escherichia coli strains by selection for a closely linked TnlO insertion by Schweizer H. (1983)
Str 0m, A. R. , P. Falkenberg , and B. Landfald . 1986 . Genetics of osmoregulation in Escherichia coli: uptake and biosynthesis of organic osmolytes . FEMS Microbiol. Rev. 39 : 79 - 86 . (10.1111/j.1574-6968.1986.tb01846.x) / FEMS Microbiol. Rev. / Genetics of osmoregulation in Escherichia coli: uptake and biosynthesis of organic osmolytes by Str A. R. (1986)
Truper , H. G. , and E. A. Galinski . 1990 . Biosynthesis and fate of compatible solutes in extremely halophilic phototrophic eubacteria . FEMS Microbiol. Rev. 75 : 247 - 254 . (10.1016/0378-1097(90)90535-X) / FEMS Microbiol. Rev. / Biosynthesis and fate of compatible solutes in extremely halophilic phototrophic eubacteria by Truper H. G. (1990)

Dates

Type	When
Created	8 years, 10 months ago (Nov. 4, 2016, 2:18 p.m.)
Deposited	4 years, 1 month ago (July 29, 2021, 1:54 p.m.)
Indexed	4 weeks, 1 day ago (Aug. 7, 2025, 5:17 p.m.)
Issued	34 years, 7 months ago (Feb. 1, 1991)
Published	34 years, 7 months ago (Feb. 1, 1991)
Published Print	34 years, 7 months ago (Feb. 1, 1991)

Funders 0

None

BibTeX

@article{Styrvold_1991, title={Synthesis, accumulation, and excretion of trehalose in osmotically stressed Escherichia coli K-12 strains: influence of amber suppressors and function of the periplasmic trehalase}, volume={173}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.173.3.1187-1192.1991}, DOI={10.1128/jb.173.3.1187-1192.1991}, number={3}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Styrvold, O B and Strøm, A R}, year={1991}, month=feb, pages={1187–1192} }

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      "journal-title": "J. Biol. Chem."
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      "DOI": "10.1128/jb.172.6.3450-3461.1990",
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      "author": "Boos W.",
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      "volume": "162",
      "author": "Bremer E.",
      "year": "1985",
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      "journal-title": "J. Bacteriol."
    },
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      "author": "Larsen P. I.",
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      "year": "1984",
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      "doi-asserted-by": "crossref",
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      "volume": "137",
      "author": "Marechal L. R.",
      "year": "1984",
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      "journal-title": "Arch. Microbiol."
    },
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      "key": "p_21",
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      "doi-asserted-by": "crossref",
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      "DOI": "10.1128/jb.161.1.393-401.1985",
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      "volume": "161",
      "author": "Perroud B.",
      "year": "1985",
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      "journal-title": "J. Bacteriol."
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      "doi-asserted-by": "crossref",
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      "volume": "170",
      "author": "Rod M. L.",
      "year": "1988",
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      "journal-title": "J. Bacteriol."
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      "volume": "192",
      "author": "Schweizer H.",
      "year": "1983",
      "unstructured": "Schweizer , H. , and W. Boos . 1983 . Transfer of the A(argFlac)U169 mutation between Escherichia coli strains by selection for a closely linked TnlO insertion . Mol. Gen. Genet. 192 : 293 - 294 .",
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    },
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      "volume": "39",
      "author": "Str A. R.",
      "year": "1986",
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      "author": "Truper H. G.",
      "year": "1990",
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