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Archives of Microbiology

, Volume 154, Issue 1, pp 60–66 | Cite as

The specific functions of menaquinone and demethylmenaquinone in anaerobic respiration with fumarate, dimethylsulfoxide, trimethylamine N-oxide and nitrate by Escherichia coli

  • U. Wissenbach
  • A. Kröger
  • G. Unden
Original Papers

Abstract

The respiratory activities of E. coli with H2 as donor and with nitrate, fumarate, dimethylsulfoxide (DMSO) or trimethylamine N-oxide (TMAO) as acceptor were measured using the membrane fraction of quinone deficient strains. The specific activities of the membrane fraction lacking naphthoquinones with fumarate, DMSO or TMAO amounted to ≤2% of those measured with the membrane fraction of the wild-type strain. After incorporation of vitamin K1 [instead of menaquinone (MK)] into the membrane fraction deficient of naphthoquinones, the activities with fumarate or DMSO were 92% or 17%, respectively, of the activities which could be theoretically achieved. Incorporation of demethylmenaquinone (DMK) did not lead to a stimulation of the activities of the mutant. In contrast, the electron transport activity with TMAO was stimulated by the incorporation of either vitamin K1 or DMK. Nitrate respiration was fully active in membrane fractions lacking either naphthoquinones or Q, but was ≤3% of the wild-type activity, when all quinones were missing. Nitrate respiration was stimulated on the incorporation of either vitamin K1 or Q into the membrane fraction lacking quinones, while the incorporation of DMK was without effect. These results suggest that MK is specifically involved in the electron transport chains catalyzing the reduction of fumarate or DMSO, while either MK or DMK serve as mediators in TMAO reduction. Nitrate respiration requires either Q or MK.

Key words

Menaquinone Demethylmenaquinone Anaerobic respiration Fumarate respiration DMSO respiration Nitrate respiration Escherichia coli 

Abbreviations

DMK

demethylmenaquinone

MK

menaquinone

Q

ubiquinone

DMSO

dimethylsulfoxide

TMAO

trimethylamine N-oxide

DMS

dimethylsulfide

TMA

trimethylamine

BV

benzylviologen

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References

  1. Ackrell BAC, Cochran B, Kearney EB, Cecchini G (1987) Redox properties of Escherichia coli fumarate reductase. In: Edmondson DE, McCormick DB (eds) Flavins and flavoproteins. Walter de Gruyter, Berlin, pp 691–694Google Scholar
  2. Bilous PT, Weiner JH (1985) Proton translocation coupled to dimethylsulfoxide reduction in anaerobically grown Escherichia coli HB101. J Bacteriol 163:369–375Google Scholar
  3. Bode CH, Goebell H, Stähler E (1968) Zur Eliminierung von Trübungsfehlern bei der Eiweißbestimmung mit der Biuretmethode. Z Klin Chem Klin Biochem 5:419–422Google Scholar
  4. Cammack R, Patil DS, Condon C, Owen P, Cole ST, Weiner JH (1985) In: Bray RC, Engel PC, Mayhew SG (eds) Flavins and flavoproteins. Walter de Gruyter, Berlin, pp 551–554Google Scholar
  5. Dickie P, Weiner JH (1979) Purification and characterization of membrane-bound fumarate reductase from anaerobically grown Escherichia coli. Can J Biochem 57:813–821Google Scholar
  6. Driessen AJM, deVrij W, Konings WN (1986) Functional incorporation of beef-heart cytochrome c oxidase into membranes of Streptococcus cremoris. Eur J Biochem 154:617–624Google Scholar
  7. Graf M, Bokranz M, Böcher R, Friedl P, Kröger A (1985) Electron transport driven phosphorylation catalyzed by proteoliposomes containing hydrogenase, fumarate reductase and ATP synthase. FEBS Lett 184:100–103Google Scholar
  8. Guest JR (1977) Menaquinone biosynthesis: Mutants of Escherichia coli K-12 requiring 2-succinylbenzoate. J Bacteriol 130:1038–1046Google Scholar
  9. Guest JR (1979) Anaerobic growth of Escherichia coli K12 with fumarate as terminal electron acceptor. Genetic studies with menaquinone and fluoro-acetate-resistent mutants. J Gen Microbiol 115:259–271Google Scholar
  10. Holländer R (1976) Correlation of the function of demethylmenaquinone in bacterial electron transport with its redox potential. FEBS Lett 72:98–100Google Scholar
  11. Ingledew WJ, Poole RK (1984) The respiratory chains of Escherichia coli. Microbiol Rev 48:222–271Google Scholar
  12. Kröger A, Klingenberg M (1973) The kinetics of the redox reactions of ubiquinone related to the electron transport activity in the respiratory chain. Eur J Biochem 34:358–368Google Scholar
  13. Kröger A, Unden G (1985) The function of menaquinone in bacterial electron transport. In: Lenaz G (ed) Coenzyme Q. John Wiley, Chichester, pp 285–300Google Scholar
  14. Kröger A, Dadák V, Klingenberg M, Diemer F (1971) On the role of quinones in bacterial electron transport: Differential roles of Ubiquinone and Menaquinone in Proteus rettgeri. Eur J Biochem 21:322–333Google Scholar
  15. Lenaz G (1988) Role of mobility of redox components in the inner mitochondrial membrane. J Membrane Biol 104:193–209Google Scholar
  16. Mannheim W, Stieler W, Wolf G, Zabel R (1978) Taxonomic significance of respiratory quinones and fumarate respiration in Actinobacillus and Pasteurella. Int J Syst Bacteriol 28:7–13Google Scholar
  17. Meganathan JR (1984) Inability of men mutants of Escherichia coli to use trimethylamine N-oxide as an electron acceptor. FEMS Microbiol Lett 24:57–62Google Scholar
  18. Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New YorkGoogle Scholar
  19. Morningstar JE, Johnson MK, Cecchini G, Ackrell BAC, Kearney EB (1985) The high potential Iron-Sulfur-Center in Escherichia coli fumarate reductase is a three-iron cluster. J Biol Chem 260:13631–13638Google Scholar
  20. Polglase WJ, Pun WT, Withaar J (1966) Lipoquinones of Escherichia coli. Biochim Biophys Acta 118:425–426Google Scholar
  21. Schnorf U (1966) Thesis, No. 3871, ETH, ZürichGoogle Scholar
  22. Takagi M, Tsuchiya T, Ishimoto M (1981) Proton translocation coupled to trimethylamine N-oxide reduction in anaerobically grown Escherichia coli. J Bacteriol 148:762–768Google Scholar
  23. Unden G (1988) Differential roles for menaquinone and demethylmenaquinone in anaerobic electron transport of E. coli and their fnr-independent expression. Arch Microbiol 150:499–503Google Scholar
  24. Unden G, Albracht SPJ, Kröger A (1984) Redoxpotential and kinetic properties of fumarate reductase complex from Vibrio succinogenes. Biochim Biophys Acta 767:460–469Google Scholar
  25. Unden G, Duchene A (1987) On the role of cyclic AMP and the Fnr protein in Escherichia coli growing anaerobically. Arch Microbiol 147:195–200Google Scholar
  26. Unden G, Hackenberg H, Kröger A (1980) Isolation and functional aspects of the fumarate reductase involved in the phosphorylative electron transport of Vibrio succinogenes. Biochim Biophys Acta 591:275–288Google Scholar
  27. Unden G, Böcher R, Knecht J, Kröger A (1982) Hydrogenase from Vibrio succinogenes, a nickel protein. FEBS Lett 145:230–234Google Scholar
  28. Wallace BJ, Young IG (1977) Role of quinones in electron transport to oxygen and nitrate in Escherichia coli. Biochim Biophys Acta 461:84–100Google Scholar
  29. Weiner JH, MacIsaac DP, Bishop RE, Bilous PT (1988) Purification and properties of Escherichia coli dimethylsulfoxide reductase, an iron-sulfur molybdoenzyme with broad substrate specificity. J Bacteriol 170:1505–1510Google Scholar
  30. Whistance GR, Threlfall DR (1968) Effect of anaerobiosis on the concentrations of demethylmenaquinone, menaquinone and ubiquinone in Escherichia freundii, Proteus mirabilis and Aeromonas punctata. Biochem J 108:505–507Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • U. Wissenbach
    • 1
  • A. Kröger
    • 1
  • G. Unden
    • 1
  1. 1.Institut für MikrobiologieJ. W. Goethe-UniversitätFrankfurt/MainFederal Republic of Germany

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