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. 1993 Oct;175(20):6671–6678. doi: 10.1128/jb.175.20.6671-6678.1993

Three overlapping lct genes involved in L-lactate utilization by Escherichia coli.

J M Dong 1, J S Taylor 1, D J Latour 1, S Iuchi 1, E C Lin 1
PMCID: PMC206779  PMID: 8407843

Abstract

In Escherichia coli, the lct locus at min 80 on the chromosome map is associated with ability to grow on L-lactate and to synthesize a substrate-inducible flavin-linked dehydrogenase. Similar to that of the glpD-encoded aerobic glycerol-3-phosphate dehydrogenase, the level of induced enzyme activity is elevated by aerobiosis. Both of these controls are mediated by the two-component signal transduction system ArcB/ArcA, although sensitivity to the control is much more striking for L-lactate dehydrogenase. This study disclosed that the lct locus contained three overlapping genes in the clockwise order of lctD (encoding a flavin mononucleotide-dependent dehydrogenase), lctR (encoding a putative regulator), and lctP (encoding a permease) on the chromosomal map. These genes, however, are transcribed in the counterclockwise direction. No homology in amino acid sequence was found between aerobic glycerol-3-phosphate dehydrogenase and L-lactate dehydrogenase. A phi (lctD-lac) mutant was inducible by L-lactate but not D-lactate. Although the mutant lost the ability to grow on L-lactate, growth on D-lactate, known to depend on a different enzyme, remained normal.

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Selected References

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  1. Allison S. L., Phillips A. T. Nucleotide sequence of the gene encoding the repressor for the histidine utilization genes of Pseudomonas putida. J Bacteriol. 1990 Sep;172(9):5470–5476. doi: 10.1128/jb.172.9.5470-5476.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Austin D., Larson T. J. Nucleotide sequence of the glpD gene encoding aerobic sn-glycerol 3-phosphate dehydrogenase of Escherichia coli K-12. J Bacteriol. 1991 Jan;173(1):101–107. doi: 10.1128/jb.173.1.101-107.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 8. Microbiol Rev. 1990 Jun;54(2):130–197. doi: 10.1128/mr.54.2.130-197.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bremer E., Silhavy T. J., Weinstock G. M. Transposable lambda placMu bacteriophages for creating lacZ operon fusions and kanamycin resistance insertions in Escherichia coli. J Bacteriol. 1985 Jun;162(3):1092–1099. doi: 10.1128/jb.162.3.1092-1099.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Buck D., Guest J. R. Overexpression and site-directed mutagenesis of the succinyl-CoA synthetase of Escherichia coli and nucleotide sequence of a gene (g30) that is adjacent to the suc operon. Biochem J. 1989 Jun 15;260(3):737–747. doi: 10.1042/bj2600737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Campbell H. D., Rogers B. L., Young I. G. Nucleotide sequence of the respiratory D-lactate dehydrogenase gene of Escherichia coli. Eur J Biochem. 1984 Oct 15;144(2):367–373. doi: 10.1111/j.1432-1033.1984.tb08473.x. [DOI] [PubMed] [Google Scholar]
  7. Chen C. M., Ye Q. Z., Zhu Z. M., Wanner B. L., Walsh C. T. Molecular biology of carbon-phosphorus bond cleavage. Cloning and sequencing of the phn (psiD) genes involved in alkylphosphonate uptake and C-P lyase activity in Escherichia coli B. J Biol Chem. 1990 Mar 15;265(8):4461–4471. [PubMed] [Google Scholar]
  8. Chen Y. M., Zhu Y., Lin E. C. The organization of the fuc regulon specifying L-fucose dissimilation in Escherichia coli K12 as determined by gene cloning. Mol Gen Genet. 1987 Dec;210(2):331–337. doi: 10.1007/BF00325702. [DOI] [PubMed] [Google Scholar]
  9. Cocks G. T., Aguilar T., Lin E. C. Evolution of L-1, 2-propanediol catabolism in Escherichia coli by recruitment of enzymes for L-fucose and L-lactate metabolism. J Bacteriol. 1974 Apr;118(1):83–88. doi: 10.1128/jb.118.1.83-88.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cole S. T., Eiglmeier K., Ahmed S., Honore N., Elmes L., Anderson W. F., Weiner J. H. Nucleotide sequence and gene-polypeptide relationships of the glpABC operon encoding the anaerobic sn-glycerol-3-phosphate dehydrogenase of Escherichia coli K-12. J Bacteriol. 1988 Jun;170(6):2448–2456. doi: 10.1128/jb.170.6.2448-2456.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DiRusso C. C. Nucleotide sequence of the fadR gene, a multifunctional regulator of fatty acid metabolism in Escherichia coli. Nucleic Acids Res. 1988 Aug 25;16(16):7995–8009. doi: 10.1093/nar/16.16.7995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fujita Y., Fujita T. Identification and nucleotide sequence of the promoter region of the Bacillus subtilis gluconate operon. Nucleic Acids Res. 1986 Feb 11;14(3):1237–1252. doi: 10.1093/nar/14.3.1237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Futai M., Kimura H. Inducible membrane-bound L-lactate dehydrogenase from Escherichia coli. Purification and properties. J Biol Chem. 1977 Aug 25;252(16):5820–5827. [PubMed] [Google Scholar]
  14. Giegel D. A., Williams C. H., Jr, Massey V. L-lactate 2-monooxygenase from Mycobacterium smegmatis. Cloning, nucleotide sequence, and primary structure homology within an enzyme family. J Biol Chem. 1990 Apr 25;265(12):6626–6632. [PubMed] [Google Scholar]
  15. Iuchi S., Lin E. C. The narL gene product activates the nitrate reductase operon and represses the fumarate reductase and trimethylamine N-oxide reductase operons in Escherichia coli. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3901–3905. doi: 10.1073/pnas.84.11.3901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Iuchi S., Lin E. C. arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc Natl Acad Sci U S A. 1988 Mar;85(6):1888–1892. doi: 10.1073/pnas.85.6.1888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kistler W. S., Lin E. C. Purification and properties of the flavine-stimulated anaerobic L- -glycerophosphate dehydrogenase of Escherichia coli. J Bacteriol. 1972 Oct;112(1):539–547. doi: 10.1128/jb.112.1.539-547.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kline E. S., Mahler H. R. The lactic dehydrogenases of E. coli. Ann N Y Acad Sci. 1965 Jul 31;119(3):905–919. doi: 10.1111/j.1749-6632.1965.tb47451.x. [DOI] [PubMed] [Google Scholar]
  19. Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
  20. Kuritzkes D. R., Zhang X. Y., Lin E. C. Use of phi(glp-lac) in studies of respiratory regulation of the Escherichia coli anaerobic sn-glycerol-3-phosphate dehydrogenase genes (glpAB). J Bacteriol. 1984 Feb;157(2):591–598. doi: 10.1128/jb.157.2.591-598.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Lederer F., Cortial S., Becam A. M., Haumont P. Y., Perez L. Complete amino acid sequence of flavocytochrome b2 from baker's yeast. Eur J Biochem. 1985 Oct 15;152(2):419–428. doi: 10.1111/j.1432-1033.1985.tb09213.x. [DOI] [PubMed] [Google Scholar]
  23. Lin R. J., Hill C. W. Mapping the xyl, mtl, and lct loci in Escherichia coli K-12. J Bacteriol. 1983 Nov;156(2):914–916. doi: 10.1128/jb.156.2.914-916.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lindqvist Y., Brändén C. I. The active site of spinach glycolate oxidase. J Biol Chem. 1989 Feb 25;264(6):3624–3628. [PubMed] [Google Scholar]
  25. Lindqvist Y. Refined structure of spinach glycolate oxidase at 2 A resolution. J Mol Biol. 1989 Sep 5;209(1):151–166. doi: 10.1016/0022-2836(89)90178-2. [DOI] [PubMed] [Google Scholar]
  26. Pascal M. C., Pichinoty F. Régulation de la biosynthèse et de la fonction des D- et L-lactate-déshydrogénases chez Aerobacter aerogenes. Biochim Biophys Acta. 1965 Jul 29;105(1):54–69. [PubMed] [Google Scholar]
  27. Pascal M. C., Puig J., Lepelletier M. Etude génétique d'une mutation affectant l'activité L-actate-déshydrogénase chez escherichia coli K 12. C R Acad Sci Hebd Seances Acad Sci D. 1969 Jan 27;268(4):737–739. [PubMed] [Google Scholar]
  28. Risler Y., Tegoni M., Gervais M. Nucleotide sequence of the Hansenula anomala gene encoding flavocytochrome b2 (L-lactate:cytochrome c oxidoreductase). Nucleic Acids Res. 1989 Oct 25;17(20):8381–8381. doi: 10.1093/nar/17.20.8381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Schwacha A., Bender R. A. Nucleotide sequence of the gene encoding the repressor for the histidine utilization genes of Klebsiella aerogenes. J Bacteriol. 1990 Sep;172(9):5477–5481. doi: 10.1128/jb.172.9.5477-5481.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Stephens P. E., Darlison M. G., Lewis H. M., Guest J. R. The pyruvate dehydrogenase complex of Escherichia coli K12. Nucleotide sequence encoding the pyruvate dehydrogenase component. Eur J Biochem. 1983 Jun 1;133(1):155–162. doi: 10.1111/j.1432-1033.1983.tb07441.x. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Toneguzzo F., Glynn S., Levi E., Mjolsness S., Hayday A. Use of a chemically modified T7 DNA polymerase for manual and automated sequencing of supercoiled DNA. Biotechniques. 1988 May;6(5):460–469. [PubMed] [Google Scholar]
  33. Tsou A. Y., Ransom S. C., Gerlt J. A., Buechter D. D., Babbitt P. C., Kenyon G. L. Mandelate pathway of Pseudomonas putida: sequence relationships involving mandelate racemase, (S)-mandelate dehydrogenase, and benzoylformate decarboxylase and expression of benzoylformate decarboxylase in Escherichia coli. Biochemistry. 1990 Oct 23;29(42):9856–9862. doi: 10.1021/bi00494a015. [DOI] [PubMed] [Google Scholar]
  34. Volokita M., Somerville C. R. The primary structure of spinach glycolate oxidase deduced from the DNA sequence of a cDNA clone. J Biol Chem. 1987 Nov 25;262(33):15825–15828. [PubMed] [Google Scholar]
  35. Xia Z. X., Shamala N., Bethge P. H., Lim L. W., Bellamy H. D., Xuong N. H., Lederer F., Mathews F. S. Three-dimensional structure of flavocytochrome b2 from baker's yeast at 3.0-A resolution. Proc Natl Acad Sci U S A. 1987 May;84(9):2629–2633. doi: 10.1073/pnas.84.9.2629. [DOI] [PMC free article] [PubMed] [Google Scholar]

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