Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1996 Nov;178(21):6233–6237. doi: 10.1128/jb.178.21.6233-6237.1996

H+/e- stoichiometry for NADH dehydrogenase I and dimethyl sulfoxide reductase in anaerobically grown Escherichia coli cells.

A V Bogachev 1, R A Murtazina 1, V P Skulachev 1
PMCID: PMC178495  PMID: 8892824

Abstract

Anaerobically grown Escherichia coli cells were shown to acidify the reaction medium in response to oxygen or dimethyl sulfoxide (DMSO) pulses, with the H+/e- stoichiometry being close to 2.5 and 1.5, respectively. In the presence of the NADH dehydrogenase I (NDH-I) inhibitor 8-methyl-N-vanillyl-6-nonenamide (capsaicin) or in mutants lacking NDH-I, this ratio decreased to 1 for O2 and to 0 for DMSO. These data suggest that (i) the H+/e- stoichiometry for E. coli NDH-I is at least 1.5 and (ii) the DMSO reductase does not generate a proton motive force.

Full Text

The Full Text of this article is available as a PDF (239.1 KB).

Selected References

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

  1. Bilous P. T., Cole S. T., Anderson W. F., Weiner J. H. Nucleotide sequence of the dmsABC operon encoding the anaerobic dimethylsulphoxide reductase of Escherichia coli. Mol Microbiol. 1988 Nov;2(6):785–795. doi: 10.1111/j.1365-2958.1988.tb00090.x. [DOI] [PubMed] [Google Scholar]
  2. Bilous P. T., Weiner J. H. Dimethyl sulfoxide reductase activity by anaerobically grown Escherichia coli HB101. J Bacteriol. 1985 Jun;162(3):1151–1155. doi: 10.1128/jb.162.3.1151-1155.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bilous P. T., Weiner J. H. Proton translocation coupled to dimethyl sulfoxide reduction in anaerobically grown Escherichia coli HB101. J Bacteriol. 1985 Jul;163(1):369–375. doi: 10.1128/jb.163.1.369-375.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bongaerts J., Zoske S., Weidner U., Unden G. Transcriptional regulation of the proton translocating NADH dehydrogenase genes (nuoA-N) of Escherichia coli by electron acceptors, electron donors and gene regulators. Mol Microbiol. 1995 May;16(3):521–534. doi: 10.1111/j.1365-2958.1995.tb02416.x. [DOI] [PubMed] [Google Scholar]
  5. Calhoun M. W., Gennis R. B. Demonstration of separate genetic loci encoding distinct membrane-bound respiratory NADH dehydrogenases in Escherichia coli. J Bacteriol. 1993 May;175(10):3013–3019. doi: 10.1128/jb.175.10.3013-3019.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cotter P. A., Chepuri V., Gennis R. B., Gunsalus R. P. Cytochrome o (cyoABCDE) and d (cydAB) oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product. J Bacteriol. 1990 Nov;172(11):6333–6338. doi: 10.1128/jb.172.11.6333-6338.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Ingledew W. J., Poole R. K. The respiratory chains of Escherichia coli. Microbiol Rev. 1984 Sep;48(3):222–271. doi: 10.1128/mr.48.3.222-271.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Iuchi S., Chepuri V., Fu H. A., Gennis R. B., Lin E. C. Requirement for terminal cytochromes in generation of the aerobic signal for the arc regulatory system in Escherichia coli: study utilizing deletions and lac fusions of cyo and cyd. J Bacteriol. 1990 Oct;172(10):6020–6025. doi: 10.1128/jb.172.10.6020-6025.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jones R. W. Hydrogen-dependent proton translocation by membrane vesicles from Escherichia coli [proceedings]. Biochem Soc Trans. 1979 Oct;7(5):1136–1137. doi: 10.1042/bst0071136. [DOI] [PubMed] [Google Scholar]
  11. Leif H., Sled V. D., Ohnishi T., Weiss H., Friedrich T. Isolation and characterization of the proton-translocating NADH: ubiquinone oxidoreductase from Escherichia coli. Eur J Biochem. 1995 Jun 1;230(2):538–548. doi: 10.1111/j.1432-1033.1995.tb20594.x. [DOI] [PubMed] [Google Scholar]
  12. Lemasters J. J., Grunwald R., Emaus R. K. Thermodynamic limits to the ATP/site stoichiometries of oxidative phosphorylation by rat liver mitochondria. J Biol Chem. 1984 Mar 10;259(5):3058–3063. [PubMed] [Google Scholar]
  13. Lin E. C., Iuchi S. Regulation of gene expression in fermentative and respiratory systems in Escherichia coli and related bacteria. Annu Rev Genet. 1991;25:361–387. doi: 10.1146/annurev.ge.25.120191.002045. [DOI] [PubMed] [Google Scholar]
  14. Matsushita K., Ohnishi T., Kaback H. R. NADH-ubiquinone oxidoreductases of the Escherichia coli aerobic respiratory chain. Biochemistry. 1987 Dec 1;26(24):7732–7737. doi: 10.1021/bi00398a029. [DOI] [PubMed] [Google Scholar]
  15. Oden K. L., DeVeaux L. C., Vibat C. R., Cronan J. E., Jr, Gennis R. B. Genomic replacement in Escherichia coli K-12 using covalently closed circular plasmid DNA. Gene. 1990 Nov 30;96(1):29–36. doi: 10.1016/0378-1119(90)90337-q. [DOI] [PubMed] [Google Scholar]
  16. Puustinen A., Finel M., Haltia T., Gennis R. B., Wikström M. Properties of the two terminal oxidases of Escherichia coli. Biochemistry. 1991 Apr 23;30(16):3936–3942. doi: 10.1021/bi00230a019. [DOI] [PubMed] [Google Scholar]
  17. Sambasivarao D., Weiner J. H. Dimethyl sulfoxide reductase of Escherichia coli: an investigation of function and assembly by use of in vivo complementation. J Bacteriol. 1991 Oct;173(19):5935–5943. doi: 10.1128/jb.173.19.5935-5943.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Skulachev V. P. Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants. Q Rev Biophys. 1996 May;29(2):169–202. doi: 10.1017/s0033583500005795. [DOI] [PubMed] [Google Scholar]
  19. Sled V. D., Friedrich T., Leif H., Weiss H., Meinhardt S. W., Fukumori Y., Calhoun M. W., Gennis R. B., Ohnishi T. Bacterial NADH-quinone oxidoreductases: iron-sulfur clusters and related problems. J Bioenerg Biomembr. 1993 Aug;25(4):347–356. doi: 10.1007/BF00762460. [DOI] [PubMed] [Google Scholar]
  20. Spiro S., Roberts R. E., Guest J. R. FNR-dependent repression of the ndh gene of Escherichia coli and metal ion requirement for FNR-regulated gene expression. Mol Microbiol. 1989 May;3(5):601–608. doi: 10.1111/j.1365-2958.1989.tb00207.x. [DOI] [PubMed] [Google Scholar]
  21. Vinogradov A. D. Kinetics, control, and mechanism of ubiquinone reduction by the mammalian respiratory chain-linked NADH-ubiquinone reductase. J Bioenerg Biomembr. 1993 Aug;25(4):367–375. doi: 10.1007/BF00762462. [DOI] [PubMed] [Google Scholar]
  22. Weiner J. H., MacIsaac D. P., Bishop R. E., Bilous P. T. Purification and properties of Escherichia coli dimethyl sulfoxide reductase, an iron-sulfur molybdoenzyme with broad substrate specificity. J Bacteriol. 1988 Apr;170(4):1505–1510. doi: 10.1128/jb.170.4.1505-1510.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Wikström M., Penttilä T. Critical evaluation of the proton-translocating property of cytochrome oxidase in rat liver mitochondria. FEBS Lett. 1982 Aug 2;144(2):183–189. doi: 10.1016/0014-5793(82)80634-0. [DOI] [PubMed] [Google Scholar]
  24. Wikström M. Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone. FEBS Lett. 1984 Apr 24;169(2):300–304. doi: 10.1016/0014-5793(84)80338-5. [DOI] [PubMed] [Google Scholar]
  25. Wissenbach U., Kröger A., Unden G. The specific functions of menaquinone and demethylmenaquinone in anaerobic respiration with fumarate, dimethylsulfoxide, trimethylamine N-oxide and nitrate by Escherichia coli. Arch Microbiol. 1990;154(1):60–66. doi: 10.1007/BF00249179. [DOI] [PubMed] [Google Scholar]
  26. Wissenbach U., Ternes D., Unden G. An Escherichia coli mutant containing only demethylmenaquinone, but no menaquinone: effects on fumarate, dimethylsulfoxide, trimethylamine N-oxide and nitrate respiration. Arch Microbiol. 1992;158(1):68–73. doi: 10.1007/BF00249068. [DOI] [PubMed] [Google Scholar]
  27. Yagi T. Inhibition by capsaicin of NADH-quinone oxidoreductases is correlated with the presence of energy-coupling site 1 in various organisms. Arch Biochem Biophys. 1990 Sep;281(2):305–311. doi: 10.1016/0003-9861(90)90448-8. [DOI] [PubMed] [Google Scholar]
  28. Young I. G., Rogers B. L., Campbell H. D., Jaworowski A., Shaw D. C. Nucleotide sequence coding for the respiratory NADH dehydrogenase of Escherichia coli. UUG initiation codon. Eur J Biochem. 1981 May;116(1):165–170. doi: 10.1111/j.1432-1033.1981.tb05314.x. [DOI] [PubMed] [Google Scholar]
  29. Zambrano M. M., Kolter R. Escherichia coli mutants lacking NADH dehydrogenase I have a competitive disadvantage in stationary phase. J Bacteriol. 1993 Sep;175(17):5642–5647. doi: 10.1128/jb.175.17.5642-5647.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES