Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Regulation of anaerobic respiratory pathways in Wolinella succinogenes by the presence of electron acceptors

Abstract

In Wolinella succinogenes ATP synthesis and consequently bacterial growth can be driven by the reduction of either nitrate (E′0=+0.42 V), nitrite (E′0=+0.36 V), fumarate (E′0=+0.03 V) or sulphur (E′0=-0.27 V) with formate as the electron donor. Bacteria growing in the presence of nitrate and fumarate were found to reduce both acceptors simultaneously, while the reduction of both nitrate and fumarate is blocked during growth with sulphur. These observations were paralleled by the presence and absence of the corresponding bacterial reductase activities. Using a specific antiserum, fumarate reductase was shown to be present in bacteria grown with fumarate and nitrate, and to be nearly absent from bacteria grown in the presence of sulphur. The contents of polysulphide reductase, too, corresponded to the enzyme activities found in the bacteria. This suggests that the activities of anaerobic respiration are regulated at the biosynthetic level in W. succinogenes. Thus nitrate and fumarate reduction are repressed by the most electronegative acceptor of anacrobic respiration, sulphur. By contrast, in Escherichia coli a similar effect is exerted by the most electropositive acceptor, O2. W. succinogenes also differs from E. coli in that fumarate reductase is not repressed by nitrate.

This is a preview of subscription content, log in to check access.

Abbreviations

BV:

benzyl viologen

DMN:

2,3-dimethyl-1,4-naphthoquinone

DMSO:

dimethylsulfoxide

TMAO:

trimethylamine-N-oxide

References

  1. BergmeyerHU (1974) Methoden der enzymatischen Analyse. Verlag Chemie, Weinheim, pp 1596–1600

  2. BodeC, GoebellH, StählerE (1968) Zur Eliminierung von Trübungsfehlern bei der Eiweißbestimmung mit der Biuretmethode. Z Klin Chem Biochem 6: 419–422

  3. BokranzM, KatzJ, SchröderI, RobertonAM, KrögerA (1983) Energy metabolism and biosynthesis of Vibrio succinogenes growing with nitrate or nitrite as terminal electron acceptor. Arch Microbiol 135: 36–41

  4. BokranzM, GutmannM, KörtnerC, KojroE, FahrenholzF, LauterbachF, KrögerA (1991) Cloning and nucleotide sequence of the structural genes encoding the formate dehydrogenase of Wolinella succinogenes. Arch Microbiol 156: 119–128

  5. DorßF, GeislerV, LengerR, KrafftT, TripierD, JuvenalK, KrögerA (1992) The quinone reactive Ni/Fe. hydrogenase of Wolinella succinogenes. Eur J Biochem 206: 93–102

  6. GunsalusRP, KalmanLV, StewartRR (1989) Nucleotide sequence of the narL gene that is involved in global regulation of nitrate controlled respiratory genes of Escherichia coli. Nucleic Acids Res 17: 1965–1975

  7. HartleyAM, AsaiRJ (1963) Spectrophotometric determination of nitrate with 2,6-xylenol reagent. Anal Chem 53: 1207–1213

  8. HowardBH, HungateRE (1976) Desulfovibrio of the sheep rumen. Appl Env Microbiol 32: 598–602

  9. KlimmekO, KrögerA, SteudelR, HoldtG (1991) Growth of Wolinella succinogenes with polysulphide as terminal acceptor of phosphorylative electron transport. Arch Microbiol 155: 177–182

  10. KrafftT, BokranzM, KlimmekO, SchröderI, FahrenholzF, KojroE, KrögerA (1992) Cloning and nucleotide sequence of the psr A gene of Wolinella succinogenes polysulphide reductase. Eur J Biochem 206: 503–510

  11. KrögerA, InnerhoferA (1976) The function of menaquinone, covalently bound FAD and iron-sulfur protein in the electron transport from formate to fumarate of Vibrio succinogenes. Eur J Biochem 69: 487–495

  12. LaemmliUK (1970) Cleavage of structural proteins during the assembly of the head of prophage T4. Nature 227: 680–685

  13. LauterbachF, KörtnerCh, TripierD, UndenG (1987) Cloning and expression of the genes of two fumarate reductase subunits from Wolinella succinogenes. Eur J Biochem 166: 447–452

  14. LauterbachF, KörtnerC, AlbrachtSPJ, UndenG, KrögerA (1990) The fumarate reductase operon of Wolinella succinogenes: sequence and expression of the frdA and frdB genes. Arch Microbiol 154: 386–393

  15. LinECC, IuchiS (1991) Regulation of gene expression in fermentative and respiratory systems in Escherichia coli and related bacteria. Annu Rev Genet 25: 361–387

  16. MacyJM, SchröderI, ThauerRK, KrögerA (1986) Growth of Wolinella succinogenes on H2S plus fumarate and on formate plus sulfur as energy sources. Arch Microbiol 144: 147–150

  17. MellH, BronderM, KrögerA (1982) Cell yields of Vibrio succinogenes growing with formate and fumarate as sole carbon and energy source in chemostat culture. Arch Microbiol 131: 224–228

  18. PfennigN, TrüperHG (1981) Isolation of members of the families Chromatiaceae and Chlorobiaceae. In: StarrMP, StolpH, TrüperHG, BalousA, SchlegelHG (eds) The prokaryotes, vol 1. Springer, New York, Berlin, Heidelberg, pp 279–289

  19. RiderBF, MellonMG (1946) Colorimetric determination of nitrite. Indust Engin Chem 18: 96–98

  20. RobertsonLA, KuenenJG, (1990) Combined heterotrophic nitrification and aerobic denitrification in Thiosphera pantotropha and other bacteria. Antonie van Leeuwenhoek 57: 139–152

  21. SchröderI, KrögerA, MacyJM (1988) Isolation of the sulphur reductase and reconstitution of the sulphur respiration of Wolinella succinogenes. Arch Microbiol 149: 572–579

  22. SpiroS, GuestJR (1991) Adaptive responses to oxygen limitation in Escherichia coli. Trends Biochem Sci 16: 310–314

  23. StewartV (1988) Nitrate respiration in relation to facultative metabolism in enterobacteria. Microbiol Rev 52: 190–232

  24. StewartV, ParalesJ, MerkelSM (1989) Structure of genes narL of the nar (nitrate reductase) locus in Escherichia coli K-12. J Bacteriol 171: 2229–2234

  25. StouthamerAH, VerseveldHWvan (1985) Stoichiometry of microbial growth. In: BullAT, DaltonH (eds) Comprehensive biotechnology. Pergamon Press, Oxford, pp 215–238

  26. TrageserM, UndenG (1989) Role of cysteine residues and metal ions in the regulatory functioning of FNR, the transcriptional regulator of anaerobic respiration in Escherichia coli. Mol Microbiol 3: 593–599

  27. UndenG, HackenbergH, KrögerA (1980) Isolation and functional aspects of the fumarate reductase involved in the phosphorylative electron transport of Vibrio succinogenes. Biochim Biophys Acta 591: 275–288

  28. UndenG, BöcherR, KnechtJ, KrögerA (1982) Hydrogenase from Vibrio succinogenes, a nickel protein. FEBS Lett 145: 230–234

  29. UndenG, TrageserM, DuchéneA (1990) Effect of positive redox potentials on the expression of anaerobic respiratory enzymes in Escherichia coli. Mol Microbiol 4: 315–319

  30. UndenG, TrageserM (1991) Oxygen regulated gene expression in Escherichia coli. control of anaerobic respiration by the FNR protein. Antonie van Leeuwenhoek 59: 65–76

  31. WloczykC, KrögerA, GöbelT, HoldtG, SteudelR (1989) The electrochemical proton potential generated by the sulphur respiration of Wolinella succinogenes. Arch Microbiol 152: 600–605

  32. WolinMJ, WolinEA, JacobsNJ (1961) Cytochrome-producing anaerobic vibrio, Vibrio succinogenes spec. nov. J Bacteriol 81: 911–917

  33. YoshinariT (1980) N2O reduction by Vibrio succinogenes. Appl Environ Microbiol 39: 81–84

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Lorenzen, J.P., Kröger, A. & Unden, G. Regulation of anaerobic respiratory pathways in Wolinella succinogenes by the presence of electron acceptors. Arch. Microbiol. 159, 477–483 (1993). https://doi.org/10.1007/BF00288597

Download citation

Key words

  • Fumarate respiration
  • Nitrate respiration
  • Polysulphide respiration
  • Anaerobic regulation
  • Wolinella succinogenes
  • Escherichia coli