Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1984 Mar;157(3):828–832. doi: 10.1128/jb.157.3.828-832.1984

Dual control of a common L-1,2-propanediol oxidoreductase by L-fucose and L-rhamnose in Escherichia coli.

Y M Chen, E C Lin
PMCID: PMC215334  PMID: 6421801

Abstract

Anaerobic growth of Escherichia coli on L-fucose or L-rhamnose as the sole source of carbon and energy depends on the regeneration of NAD from NADH by disposing the intermediate L-lactaldehyde as L-1,2-propanediol. The two parallel pathways, with their own permeases and enzymes encoded by two widely separated gene clusters, appear to share a single enzyme that catalyzes the formation of L-1,2-propanediol. Although this oxidoreductase is encoded by a gene at the fuc locus, the enzyme is inducible by both L-fucose and L-rhamnose. The inducibility by L-rhamnose is controlled by a gene at the rha locus with no other known functions, since the aerobic growth rate on L-rhamnose remains normal. L-1,2-Propanediol oxidoreductase activity is inducible only anaerobically, and the effect of the two methylpentoses operates at different levels: L-fucose exerts its influence post-transcriptionally; L-rhamnose exerts its influence transcriptionally.

Full text

PDF
828

Selected References

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

  1. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 7. Microbiol Rev. 1983 Jun;47(2):180–230. doi: 10.1128/mr.47.2.180-230.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Backman K., Chen Y. M., Magasanik B. Physical and genetic characterization of the glnA--glnG region of the Escherichia coli chromosome. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3743–3747. doi: 10.1073/pnas.78.6.3743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Boronat A., Aguilar J. Metabolism of L-fucose and L-rhamnose in Escherichia coli: differences in induction of propanediol oxidoreductase. J Bacteriol. 1981 Jul;147(1):181–185. doi: 10.1128/jb.147.1.181-185.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boronat A., Aguilar J. Rhamnose-induced propanediol oxidoreductase in Escherichia coli: purification, properties, and comparison with the fucose-induced enzyme. J Bacteriol. 1979 Nov;140(2):320–326. doi: 10.1128/jb.140.2.320-326.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. CHIU T. H., FEINGOLD D. S. SUBSTRATE SPECIFICITY OF L-RHAMNULOSE 1-PHOSPHATE ADOLASE. Biochem Biophys Res Commun. 1965 May 3;19:511–516. doi: 10.1016/0006-291x(65)90155-5. [DOI] [PubMed] [Google Scholar]
  6. CHIU T. H., FEINGOLD D. S. THE PURIFICATION AND PROPERTIES OF L-RHAMNULOKINASE. Biochim Biophys Acta. 1964 Dec 23;92:489–497. doi: 10.1016/0926-6569(64)90009-4. [DOI] [PubMed] [Google Scholar]
  7. Casadaban M. J., Cohen S. N. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4530–4533. doi: 10.1073/pnas.76.9.4530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Casadaban M. J. Regulation of the regulatory gene for the arabinose pathway, araC. J Mol Biol. 1976 Jul 5;104(3):557–566. doi: 10.1016/0022-2836(76)90120-0. [DOI] [PubMed] [Google Scholar]
  9. Chen Y. M., Lin E. C. Post-transcriptional control of L-1,2-propanediol oxidoreductase in the L-fucose pathway of Escherichia coli K-12. J Bacteriol. 1984 Jan;157(1):341–344. doi: 10.1128/jb.157.1.341-344.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Chen Y. M., Lin E. C., Ros J., Aguilar J. Use of operon fusions to examine the regulation of the L-1,2-propanediol oxidoreductase gene of the fucose system in Escherichia coli K12. J Gen Microbiol. 1983 Nov;129(11):3355–3362. doi: 10.1099/00221287-129-11-3355. [DOI] [PubMed] [Google Scholar]
  11. Chiu T. H., Feingold D. S. L-rhamnulose 1-phosphate aldolase from Escherichia coli. Crystallization and properties. Biochemistry. 1969 Jan;8(1):98–108. doi: 10.1021/bi00829a015. [DOI] [PubMed] [Google Scholar]
  12. DISCHE Z., BORENFREUND E. A new spectrophotometric method for the detection and determination of keto sugars and trioses. J Biol Chem. 1951 Oct;192(2):583–587. [PubMed] [Google Scholar]
  13. Daldal F., Fraenkel D. G. Assessment of a futile cycle involving reconversion of fructose 6-phosphate to fructose 1,6-bisphosphate during gluconeogenic growth of Escherichia coli. J Bacteriol. 1983 Jan;153(1):390–394. doi: 10.1128/jb.153.1.390-394.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Debarbouille M., Schwartz M. The use of gene fusions to study the expression of malT the positive regulator gene of the maltose regulon. J Mol Biol. 1979 Aug 15;132(3):521–534. doi: 10.1016/0022-2836(79)90273-0. [DOI] [PubMed] [Google Scholar]
  15. FALKOW S., SCHNEIDER H., BARON L. S., FORMAL S. B. VIRULENCE OF ESCHERICHIA-SHIGELLA GENETIC HYBRIDS FOR THE GUINEA PIG. J Bacteriol. 1963 Dec;86:1251–1258. doi: 10.1128/jb.86.6.1251-1258.1963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. GHALAMBOR M. A., HEATH E. C. The metabolism of L-fucose. II. The enzymatic cleavage of L-fuculose 1-phosphate. J Biol Chem. 1962 Aug;237:2427–2433. [PubMed] [Google Scholar]
  17. GREEN M., COHEN S. S. Enzymatic conversion of L-fucose to L-fuculose. J Biol Chem. 1956 Apr;219(2):557–568. [PubMed] [Google Scholar]
  18. HEATH E. C., GHALAMBOR M. A. The metabolism of L-fucose. I. The purification and properties of L-fuculose kinase. J Biol Chem. 1962 Aug;237:2423–2426. [PubMed] [Google Scholar]
  19. Hacking A. J., Aguilar J., Lin E. C. Evolution of propanediol utilization in Escherichia coli: mutant with improved substrate-scavenging power. J Bacteriol. 1978 Nov;136(2):522–530. doi: 10.1128/jb.136.2.522-530.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hacking A. J., Lin E. C. Disruption of the fucose pathway as a consequence of genetic adaptation to propanediol as a carbon source in Escherichia coli. J Bacteriol. 1976 Jun;126(3):1166–1172. doi: 10.1128/jb.126.3.1166-1172.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hacking A. J., Lin E. C. Regulatory changes in the fucose system associated with the evolution of a catabolic pathway for propanediol in Escherichia coli. J Bacteriol. 1977 May;130(2):832–838. doi: 10.1128/jb.130.2.832-838.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Komeda Y., Iino T. Regulation of expression of the flagellin gene (hag) in Escherichia coli K-12: analysis of hag-lac gene fusions. J Bacteriol. 1979 Sep;139(3):721–729. doi: 10.1128/jb.139.3.721-729.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  24. LURIA S. E., ADAMS J. N., TING R. C. Transduction of lactose-utilizing ability among strains of E. coli and S. dysenteriae and the properties of the transducing phage particles. Virology. 1960 Nov;12:348–390. doi: 10.1016/0042-6822(60)90161-6. [DOI] [PubMed] [Google Scholar]
  25. LeBlanc D. J., Mortlock R. P. Metabolism of D-arabinose: a new pathway in Escherichia coli. J Bacteriol. 1971 Apr;106(1):90–96. doi: 10.1128/jb.106.1.90-96.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Power J. The L-rhamnose genetic system in Escherichia coli K-12. Genetics. 1967 Mar;55(3):557–568. doi: 10.1093/genetics/55.3.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Riley M., Anilionis A. Evolution of the bacterial genome. Annu Rev Microbiol. 1978;32:519–560. doi: 10.1146/annurev.mi.32.100178.002511. [DOI] [PubMed] [Google Scholar]
  28. SAWADA H., TAKAGI Y. THE METABOLISM OF L-RHAMNOSE IN ESCHERICHIA COLI. 3. L-RHAMULOSE-PHOSPHATE ALDOLASE. Biochim Biophys Acta. 1964 Oct 23;92:26–32. doi: 10.1016/0926-6569(64)90265-2. [DOI] [PubMed] [Google Scholar]
  29. Skjold A. C., Ezekiel D. H. Analysis of lambda insertions in the fucose utilization region of Escherichia coli K-12: use of lambda fuc and lambda argA transducing bacteriophages to partially order the fucose utilization genes. J Bacteriol. 1982 Oct;152(1):120–125. doi: 10.1128/jb.152.1.120-125.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Skjold A. C., Ezekiel D. H. Regulation of D-arabinose utilization in Escherichia coli K-12. J Bacteriol. 1982 Oct;152(1):521–523. doi: 10.1128/jb.152.1.521-523.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sridhara S., Wu T. T., Chused T. M., Lin E. C. Ferrous-activated nicotinamide adenine dinucleotide-linked dehydrogenase from a mutant of Escherichia coli capable of growth on 1, 2-propanediol. J Bacteriol. 1969 Apr;98(1):87–95. doi: 10.1128/jb.98.1.87-95.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sridhara S., Wu T. T. Purification and properties of lactaldehyde dehydrogenase from Escherichia coli. J Biol Chem. 1969 Oct 10;244(19):5233–5238. [PubMed] [Google Scholar]
  33. TAKAGI Y., SAWADA H. THE METABOLISM OF L-RHAMNOSE IN ESCHERICHIA COLI. I. L-RHAMNOSE ISOMERASE. Biochim Biophys Acta. 1964 Oct 23;92:10–17. doi: 10.1016/0926-6569(64)90263-9. [DOI] [PubMed] [Google Scholar]
  34. TAKAGI Y., SAWADA H. THE METABOLISM OF L-RHAMNOSE IN ESCHERICHIA COLI. II. L-RHAMNULOSE KINASE. Biochim Biophys Acta. 1964 Oct 23;92:18–25. doi: 10.1016/0926-6569(64)90264-0. [DOI] [PubMed] [Google Scholar]
  35. Tanaka S., Lerner S. A., Lin E. C. Replacement of a phosphoenolpyruvate-dependent phosphotransferase by a nicotinamide adenine dinucleotide-linked dehydrogenase for the utilization of mannitol. J Bacteriol. 1967 Feb;93(2):642–648. doi: 10.1128/jb.93.2.642-648.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. WILSON D. M., AJL S. Metabolism of L-rhamnose by Escherichia coli. I. L-rhamnose isomerase. J Bacteriol. 1957 Mar;73(3):410–414. doi: 10.1128/jb.73.3.410-414.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. WILSON D. M., AJL S. Metabolism of L-rhamnose by Escherichia coli. II. The phosphorylation of L-rhamnulose. J Bacteriol. 1957 Mar;73(3):415–420. doi: 10.1128/jb.73.3.415-420.1957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Zagalak B., Frey P. A., Karabatsos G. L., Abeles R. H. The stereochemistry of the conversion of D and L 1,2-propanediols to propionaldehyde. J Biol Chem. 1966 Jul 10;241(13):3028–3035. [PubMed] [Google Scholar]

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

RESOURCES