Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 Nov;177(22):6652–6656. doi: 10.1128/jb.177.22.6652-6656.1995

Regulation of malate dehydrogenase (mdh) gene expression in Escherichia coli in response to oxygen, carbon, and heme availability.

S J Park 1, P A Cotter 1, R P Gunsalus 1
PMCID: PMC177521  PMID: 7592446

Abstract

Malate dehydrogenase catalyzes the interconversion of malate and oxaloacetate. It participates as a member of the tricarboxylic acid cycle and the branched noncyclic pathways under aerobic and anaerobic cell growth conditions, respectively. To investigate how the mdh gene is expressed under these different conditions, an mdh-lacZ operon fusion was constructed and analyzed in vivo. The mdh-lacZ fusion was expressed about twofold higher under aerobic conditions than under anaerobic cell growth conditions on most media tested. This anaerobic response is modulated by the ArcA protein, which functions as a repressor of mdh gene expression under both aerobic and anaerobic conditions. In contrast, mutations in the fnr gene did not affect mdh gene expression. Interestingly, cells grown anaerobically with glycerol and trimethylamine N-oxide or fumarate showed higher levels of mdh expression than did cells that were grown aerobically. Depending on the type of carbon compound used for cell growth, mdh expression varied by 11-fold and 5-fold under aerobic and anaerobic conditions, respectively. While mdh transcription was shown to be inversely proportional to the cell growth rate, cellular heme limitation stimulated a fivefold increase in mdh gene expression. The mdh gene appears to be highly regulated to adapt to changing conditions of aerobic and anaerobic cell growth with various types of carbon substrates.

Full Text

The Full Text of this article is available as a PDF (195.2 KB).

Selected References

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

  1. Amarasingham C. R., Davis B. D. Regulation of alpha-ketoglutarate dehydrogenase formation in Escherichia coli. J Biol Chem. 1965 Sep;240(9):3664–3668. [PubMed] [Google Scholar]
  2. Chiang R. C., Cavicchioli R., Gunsalus R. P. Identification and characterization of narQ, a second nitrate sensor for nitrate-dependent gene regulation in Escherichia coli. Mol Microbiol. 1992 Jul;6(14):1913–1923. doi: 10.1111/j.1365-2958.1992.tb01364.x. [DOI] [PubMed] [Google Scholar]
  3. Cotter P. A., Gunsalus R. P. Contribution of the fnr and arcA gene products in coordinate regulation of cytochrome o and d oxidase (cyoABCDE and cydAB) genes in Escherichia coli. FEMS Microbiol Lett. 1992 Feb 1;70(1):31–36. doi: 10.1016/0378-1097(92)90558-6. [DOI] [PubMed] [Google Scholar]
  4. Cotter P. A., Gunsalus R. P. Oxygen, nitrate, and molybdenum regulation of dmsABC gene expression in Escherichia coli. J Bacteriol. 1989 Jul;171(7):3817–3823. doi: 10.1128/jb.171.7.3817-3823.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Darie S., Gunsalus R. P. Effect of heme and oxygen availability on hemA gene expression in Escherichia coli: role of the fnr, arcA, and himA gene products. J Bacteriol. 1994 Sep;176(17):5270–5276. doi: 10.1128/jb.176.17.5270-5276.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gray C. T., Wimpenny J. W., Mossman M. R. Regulation of metabolism in facultative bacteria. II. Effects of aerobiosis, anaerobiosis and nutrition on the formation of Krebs cycle enzymes in Escherichia coli. Biochim Biophys Acta. 1966 Mar 28;117(1):33–41. doi: 10.1016/0304-4165(66)90149-8. [DOI] [PubMed] [Google Scholar]
  7. Gunsalus R. P., Park S. J. Aerobic-anaerobic gene regulation in Escherichia coli: control by the ArcAB and Fnr regulons. Res Microbiol. 1994 Jun-Aug;145(5-6):437–450. doi: 10.1016/0923-2508(94)90092-2. [DOI] [PubMed] [Google Scholar]
  8. Heard J. T., Jr, Butler M. A., Baptist J. N., Matney T. S. Chromosomal location of mutations affecting the electrophoretic mobility of malate dehydrogenase in Escherichia coli K-12. J Bacteriol. 1975 Apr;122(1):329–331. doi: 10.1128/jb.122.1.329-331.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Iuchi S., Aristarkhov A., Dong J. M., Taylor J. S., Lin E. C. Effects of nitrate respiration on expression of the Arc-controlled operons encoding succinate dehydrogenase and flavin-linked L-lactate dehydrogenase. J Bacteriol. 1994 Mar;176(6):1695–1701. doi: 10.1128/jb.176.6.1695-1701.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. McAlister-Henn L., Blaber M., Bradshaw R. A., Nisco S. J. Complete nucleotide sequence of the Escherichia coli gene encoding malate dehydrogenase. Nucleic Acids Res. 1987 Jun 25;15(12):4993–4993. doi: 10.1093/nar/15.12.4993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Murphey W. H., Barnaby C., Lin F. J., Kaplan N. O. Malate dehydrogenases. II. Purification and properties of Bacillus subtilis, Bacillus stearothermophilus, and Escherichia coli malate dehydrogenases. J Biol Chem. 1967 Apr 10;242(7):1548–1559. [PubMed] [Google Scholar]
  13. Murphey W. H., Kitto G. B., Everse J., Kaplan N. Malate dehydrogenases. I. A survey of molecular size measured by gel filtration. Biochemistry. 1967 Feb;6(2):603–610. doi: 10.1021/bi00854a031. [DOI] [PubMed] [Google Scholar]
  14. Park S. J., McCabe J., Turna J., Gunsalus R. P. Regulation of the citrate synthase (gltA) gene of Escherichia coli in response to anaerobiosis and carbon supply: role of the arcA gene product. J Bacteriol. 1994 Aug;176(16):5086–5092. doi: 10.1128/jb.176.16.5086-5092.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Park S. J., Tseng C. P., Gunsalus R. P. Regulation of succinate dehydrogenase (sdhCDAB) operon expression in Escherichia coli in response to carbon supply and anaerobiosis: role of ArcA and Fnr. Mol Microbiol. 1995 Feb;15(3):473–482. doi: 10.1111/j.1365-2958.1995.tb02261.x. [DOI] [PubMed] [Google Scholar]
  16. Ramseier T. M., Nègre D., Cortay J. C., Scarabel M., Cozzone A. J., Saier M. H., Jr In vitro binding of the pleiotropic transcriptional regulatory protein, FruR, to the fru, pps, ace, pts and icd operons of Escherichia coli and Salmonella typhimurium. J Mol Biol. 1993 Nov 5;234(1):28–44. doi: 10.1006/jmbi.1993.1561. [DOI] [PubMed] [Google Scholar]
  17. Simons R. W., Houman F., Kleckner N. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene. 1987;53(1):85–96. doi: 10.1016/0378-1119(87)90095-3. [DOI] [PubMed] [Google Scholar]
  18. Sutherland P., McAlister-Henn L. Isolation and expression of the Escherichia coli gene encoding malate dehydrogenase. J Bacteriol. 1985 Sep;163(3):1074–1079. doi: 10.1128/jb.163.3.1074-1079.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Vogel R. F., Entian K. D., Mecke D. Cloning and sequence of the mdh structural gene of Escherichia coli coding for malate dehydrogenase. Arch Microbiol. 1987;149(1):36–42. doi: 10.1007/BF00423133. [DOI] [PubMed] [Google Scholar]

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

RESOURCES