Skip to main content
Log in

Energetic aspects of growth of Paracoccus denitrificans: oxygen-limitation and shift from anaerobic nitrate-limination to aerobic succinate-limitation

Evidence for a new alternative oxidase, cytochrome a 1

  • Original Papers
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

1. Growth yields and efficiency of energy conservation were the same for aerobic succinate-limited and oxygen-limited cells of Paracoccus denitrificans. 2. A shift from anaerobic nitrate-limitation to aerobic succinatelimitation showed that before and after the shift cells grew with the same capacity of energy conservation. 3. Respiration-driven proton translocation showed the presence of H+-translocating sites 1 and 2, which translocate respectively 2–3 and 4 protons per 2 electrons in oxygen-, anaerobic nitrate-and aerobic succinate-limited cells. 4. Cytochrome spectra and flash-photolysis spectra of oxygen- and nitrate-limited cells gave evidence for the presence of an alternative oxidase, cytochrome a 1, never before recognized in Paracoccus denitrificans. 5. Only a-type cytochromes liganded with CO could be flash-photolysed. No evidence for a functional cytochrome o was found in photolysis experiments. 6. Fast oxidation, before photolysis, of the bc-pool after introduction of oxygen in a CO-liganded sample at-20° to-30° C, indicated the presence of a cytochrome oxidase other than cytochrome a 1 with a very high affinity for oxygen and a low affinity for CO. 7. In photochemical action spectra, light released CO-inhibition of respiration, but the release was independent of the wavelength used (560–610 nm).

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

TMPD:

N,N,N′,N′-tetramethyl-p-phenylenediamine

References

  • Albracht SPJ, van Verseveld HW, Hagen WR, Kalkman ML (1980) A comparison of the respiratory chain in particles from Paracoccus denitrificans and bovine heart mitochondria by EPR spectroscopy. Biochim Biophys Acta 593:173–186

    Google Scholar 

  • Alefounder PR, Ferguson SJ (1980) The location of dissimilatory nitrite reductase and the control of dissimilatory nitrate reductase by oxygen in Paracoccus denitrificans. Biochem J 192:231–240

    Google Scholar 

  • Boogerd FC, van Verseveld HW, Stouthamer AH (1980) Electron transport to nitrous oxide in Paracoccus denitrificans. FEBS Microbiol Lett 113:279–284

    Google Scholar 

  • Boogerd FC, van Verseveld HW, Stouthamer AH (1981) Respiration driven proton translocation with nitrite and nitrous oxide in Paracoccus denitrificans. Biochim Biophys Acta 638:181–191

    Google Scholar 

  • Castor LN, Chance B (1959) Photochemical determinations of the oxidases in bacteria. J Biol Chem 234:1587–1592

    Google Scholar 

  • Chance B, Saronio C, Leigh JS (1975) Functional intermediates in the reaction of membrane bound oxidase with oxygen. J Biol Chem 250:9226–9237

    Google Scholar 

  • Chang JP, Morris JG (1962) Studies on the utilization of nitrate by Micrococcus denitrificans. J Gen Microbiol 29:301–310

    Google Scholar 

  • Cypionka H, Meyer O (1982) Influence of carbon monoxide on growth and respiration of carbodoxybacteria and other microorganisms. FEMS Microbiol Lett 15:209–214

    Google Scholar 

  • Edwards C, Beer S, Siviram A, Chance B (1981) Photochemical action spectra of bacterial a and o-type oxidases using a dye laser. FEBS Microbiol Lett 128:205–207

    Google Scholar 

  • Forget P, DerVartanian DV (1972) The bacterial nitrate reductases: EPR studies on nitrate reductase A from Micrococcus denitrificans. Biochim Biophys Acta 256:600–606

    Google Scholar 

  • Henry MF, de Fonseka K, Chance B, Vignais PM (1979) Low temperature kinetics of terminal oxidases in Paracoccus denitrificans. Proc Int Congr Biochem 11th, Abstract 06-3-R82

  • Ingledew WJ (1977) Cytochrome a 1 as an oxidase? In: Degn H, Lloyd D, Hill GC (eds) Functions of alternative terminal oxidases, Pergamon Press, Oxford, UK, pp 79–88

    Google Scholar 

  • John P, Whatley FR (1970) Oxidative phosphorylation coupled to oxygen uptake and nitrate reduction in Micrococcus denitrificans. Biochim Biophys Acta 216:342–352

    Google Scholar 

  • John P, Whatley FR (1975) Paracoccus denitrificans and the evolutionary origin of the mitochondrion. Nature (Lond) 254:495–498

    Google Scholar 

  • Keilin D (1966) The history of cell respiration and cytochrome. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Kraayenhof R, Schuurmans JJ, Valkier LJ, Veen JPC, Marum P van, Jasper CGG (1982) A thermoelectrically regulated multipurpose cuvette for simultaneous time-dependent measurements. Anal Biochem 127:93–99

    Google Scholar 

  • Krab K, van Verseveld HW, Boogerd FC (1981) Energy conservation in aerobically and anaerobically grown Paracoccus denitrificans. The role of cytochrome c oxidase. In: Palmieri F, Quagliariello E, Silliprandi N, Slater EC (eds) Vectorial reactions in electron and ion transport in mitochondria and bacteria. Elsevier/North Holland Biomedical Press, Amsterdam

    Google Scholar 

  • Kristjansson JK, Hollocher TC (1981) Partial purification and characterization of nitrous oxide reductase from Paracoccus denitrificans. Curr Microbiol 6:247–251

    Google Scholar 

  • Kula T, Stellwagen E, Szentirmary R Kuwana T (1981) Midpoint potentials of cytochromes in vesicles of anaerobically grown Paracoccus denitrificans determined by the indirect-coulometric method. Biochim Biophys Acta 634:279–288

    Google Scholar 

  • Lam Y, Nicholas DJD (1969) Aerobic and anaerobic respiration in Micrococcus denitrificans. Biochim Biophys Acta 172:450–461

    Google Scholar 

  • Lawford HG (1978) Energy transduction in the mitochondrion-like bacterium Paracoccus denitrificans during carbon- or sulphatelimited growth in continuous culture. Can J Biochem 56:13–22

    Google Scholar 

  • Lawford HG, Cox JC, Garland PB, Haddock BA (1976) Electron transport in aerobically grown Paracoccus denitrificans: kinetic characterization of the membrane bound cytochromes and the stoichiometry of respiration driven proton translocation. FEBS Microbiol Lett 64:369–374

    Google Scholar 

  • Ludwig B (1980) Heme aa 3-type cytochrome c oxidase from bacteria. Biochim Biophys Acta 594:177–189

    Google Scholar 

  • Meijer EM, van Verseveld HW, van der Beek EG, Stouthamer AH (1977) Energy conservation during aerobic growth in Paracoccus denitrificans. Arch Microbiol 112:25–34

    Google Scholar 

  • Meijer EM, van der Zwaan JW, Stouthamer AH (1979) Location of the proton consuming site in nitrite reduction and stoichiometries for proton pumping in anaerobically grown Paracoccus denitrificans. FEMS Microbiol Lett 5:369–372

    Google Scholar 

  • Newton N (1969) The two heam nitrite reductase of Micrococcus denitrificans. Biochim Biophys Acta 185:316–331

    Google Scholar 

  • Papa S (1976) Proton translocation reactions in the respiratory chains. Biochim Biophys Acta 456:39–84

    Google Scholar 

  • Payne WJ (1973) Reduction of nitrogenous oxides by microorganisms. Bacteriol Rev 37:409–552

    Google Scholar 

  • Pichinoty F (1973) La réduction bactérienne des composés oxygènes mineraux de l'azote. Bull Inst Pasteur 71:317–395

    Google Scholar 

  • Pirt SJ (1965) The maintenance energy of bacteria in growing cultures. Proc Roy Soc B 163:224–231

    Google Scholar 

  • Poole RK, Sivaram A, Salmon I, Chance B (1982) Photolysis at very low temperatures of CO-liganded cytochrome oxidase (cytochrome d) in oxygen-limited Escherichia coli. FEBS Lett 141:237–241

    Google Scholar 

  • Poole RK, Waring AJ, Chance B (1979) The reaction of cytochrome o in Escherichia coli with oxygen. Biochem J 184:379–389

    Google Scholar 

  • Scholes P, Smith L (1968) Composition and properties of the membrane bound respiratory chain system of Micrococcus denitrificans. Biochim Biophys Acta 153:363–375

    Google Scholar 

  • Solioz M, Carafoli E, Ludwig B (1981) The cytochrome c oxidase of Paracoccus denitrificans pumps protons in a reconstituted system. J Biol Chem 257:1579–1582

    Google Scholar 

  • Stouthamer AH, Bettenhausen C (1973) Utilization of energy for growth and maintenance in continuous and batch cultures of microorganisms. Biochim Biophys Acta 301:53–70

    Google Scholar 

  • Stouthamer AH, Bettenhausen C (1975) Defermination of the efficiency of oxidative phosphorylation in continuous cultures of Aerobacter aerogenes. Arch Microbiol 102:187–192

    Google Scholar 

  • Tait GH (1975) The identification and biosynthesis of siderochromes formed by Micrococcus denitrificans. Biochem J 146:191–204

    Google Scholar 

  • van Verseveld HW, Boon JP, Stouthamer AH (1979) Growth yields and the efficiency of oxidative phosphorylation of Paracoccus denitrificans during two- (carbon) substrate-limited growth. Arch Microbiol 121:213–223

    Google Scholar 

  • van Verseveld HW, Krab K, Stouthamer AH (1981) Proton pump coupled to cytochrome c oxidase in Paracoccus denitrificans. Biochim Biophys Acta 635:525–534

    Google Scholar 

  • van Verseveld HW, Stouthamer AH (1976) Oxidative phosphorylation in Micrococcus denitrificans. Calculation of the P/O ratio in growing cells. Arch Microbiol 107:241–247

    Google Scholar 

  • van Verseveld HW, Stouthamer AH (1978a) Growth yields and the efficiency of oxidative phosphorylation during autotrophic growth of Paracoccus denitrificans on methanol and formate. Arch Microbiol 118:21–26

    Google Scholar 

  • van Verseveld HW, Stouthamer AH (1978b) Electron transport chain and coupled oxidative phosphorylation in methanol-grown Paracoccus denitrificans. Arch Microbiol 118:13–20

    Google Scholar 

  • Vignais PM, Henry MF, Sim E, Kell DB (1982) The electron transport system and hydrogenase of Paracoccus denitrificans. Curr Top Bioenerg 12:115–196

    Google Scholar 

  • de Vries W, Stouthamer AH (1968) Fermentation of glucose, lactose, galactose, mannitol and xylose by Bifidobacteria. J Bacteriol 96: 472–478

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

van Verseveld, H.W., Braster, M., Boogerd, F.C. et al. Energetic aspects of growth of Paracoccus denitrificans: oxygen-limitation and shift from anaerobic nitrate-limination to aerobic succinate-limitation. Arch Microbiol 135, 229–236 (1983). https://doi.org/10.1007/BF00414485

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00414485

Key words

Navigation