Energy conservation during aerobic growth in Paracoccus denitrificans

Paracoccus denitrificans was aerobically grown in chemostat culture with succinate or gluconate as carbon source. Due to the presence of two phosphorylation sites in the respiratory chain and the absence of branching, theoretical P/O ratios of 1.71 and 1.82 were calculated for cells growing respectively with succinate and gluconate as carbon source. Using these data, 95% confidence intervals for the P/O ratio were determined, via a mathematical model, at 0.91–1.15 and 1.00–1.37 for sulphate-limited cultures, with respectively succinate and gluconate as carbon source.These results and measurements of P/O ratios in membrane particles and of proton translocation in whole cells have led to the conclusion that site I phosphorylation is affected under sulphate-limited conditions.Under conditions of carbon source-limitation the endogenous →H+/O ratio is about 7–8. Average values of 3.40 and 4.78 were respectively found for sulphate-limited succinate- and gluconate grown cells. For starved cells, oxidizing succinate as exogenous substrate, the →H+/O ratios were determined at about 3–4, independent of the growth limiting factor. It is concluded that the number of protons ejected per pair of electrons per energy-conserving site (→H+/site ratio) is about 3–4, instead of 2 as postulated by the chemiosmotic hypothesis.

[1]  S. Hestrin.  The reaction of acetylcholine and other carboxylic acid derivatives with hydroxylamine, and its analytical application. , 1949, The Journal of biological chemistry.

[2]  P. Simonpiétri,et al.  Uncoupling in Bacterial Growth: Effect of Pantothenate Starvation on Growth of Zymomonas mobilis , 1972 .

[3]  A. H. Stouthamer,et al.  A quantitative description of heterotrophic growth in micro-organisms. , 1976, Journal of theoretical biology.

[4]  A. H. Stouthamer,et al.  A method for the determination of confidence limits for the P/2e− ratio for chosen values of YATPmax from the results of continuous culture experiments , 1977, Archives of Microbiology.

[5]  H. Lawford,et al.  Respiration-driven proton translocation in Escherichia coli. , 1973, The Biochemical journal.

[6]  J. Senez.  Some considerations on the energetics of bacterial growth. , 1962, Bacteriological reviews.

[7]  H. Witt.  10 – Primary Acts of Energy Conservation in the Functional Membrane of Photosynthesis , 1975 .

[8]  P. Mitchell.  CHEMIOSMOTIC COUPLING IN OXIDATIVE AND PHOTOSYNTHETIC PHOSPHORYLATION , 1966, Biological reviews of the Cambridge Philosophical Society.

[9]  PETER MITCHELL,et al.  Stoichiometry of Proton Translocation through the Respiratory Chain and Adenosine Triphosphatase Systems of Rat Liver Mitochondria , 1965, Nature.

[10]  H. Lawford,et al.  Electron transport in aerobically grown Paracoccus denitrificans: Kinetic characterization of the membrane‐bound cytochromes and the stoichiometry of respiration‐driven proton translocation , 1976, FEBS letters.

[11]  S. Papa,et al.  Proton translocation reactions in the respiratory chains. , 1976, Biochimica et biophysica acta.

[12]  P. Scholes,et al.  Purification and properties of a c-type cytochrome from Micrococcus denitrificans. , 1971, Biochemistry.

[13]  R. Sato,et al.  Oxidative phosphorylation in Micrococcus denitrificans. V. Effects of iron deficiency on respiratory components and oxidative phosphorylation. , 1968, Journal of biochemistry.

[14]  D. Walker,et al.  The generation and utilization of energy during growth. , 1971, Advances in microbial physiology.

[15]  A. Lehninger,et al.  Stoichiometric relationship between energy-dependent proton ejection and electron transport in mitochondria. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[16]  D. Tempest,et al.  The regulation of carbohydrate metabolism in Klebsiella aerogenes NCTC 418 organisms, growing in chemostat culture , 1975, Archives of Microbiology.

[17]  A. H. Stouthamer,et al.  Fermentation of Glucose, Lactose, Galactose, Mannitol, and Xylose by Bifidobacteria , 1968, Journal of bacteriology.

[18]  A. H. Stouthamer,et al.  Oxidative phosphorylation in Micrococcus denitrificans , 1976, Archives of Microbiology.

[19]  A. H. Stouthamer,et al.  Energy conservation during nitrate respiration in Paracoccus denitrificans , 1977, Archives of Microbiology.

[20]  P. Garland,et al.  Effect of sulphate-limited growth on mitochondrial electron transfer and energy conservation between reduced nicotinamide-adenine dinucleotide and the cytochromes in Torulopsis utilis. , 1971, The Biochemical journal.

[21]  K. Knobloch,et al.  Oxidative phosphorylation in Micrococcus denitrificans under autotrophic growth conditions , 2004, Archiv für Mikrobiologie.

[22]  H. Lawford,et al.  Respiration-driven proton translocation in Escherichia coli (Short Communication) , 1973 .

[23]  J. G. Morris,et al.  Studies on the utilization of nitrate by Micrococcus denitrificans. , 1962, Journal of general microbiology.

[24]  H. Witt.  PRIMARY ACTS OF ENERGY CONSERVATION IN THE FUNCTIONAL MEMBRANE OF PHOTOSYNTHESIS , 1974, Annals of the New York Academy of Sciences.

[25]  J. M. Brice,et al.  Bacterial respiration-linked proton translocation and its relationship to respiratory-chain composition. , 1975, European journal of biochemistry.

[26]  P. C. Hinkle,et al.  Oxidative phosphorylation and proton translocation in membrane vesicles prepared from Escherichia coli. , 1974, Biochemical and biophysical research communications.

[27]  D. Tempest,et al.  Bioenergetic aspects of aerobic growth of Klebsiella aerogenes NCTC 418 in carbon-limited and carbon-sufficient chemostat culture , 1976, Archives of Microbiology.

[28]  P. Mitchell.  Coupling of Phosphorylation to Electron and Hydrogen Transfer by a Chemi-Osmotic type of Mechanism , 1961, Nature.

[29]  R. Sato,et al.  Oxidative phosphorylation in Micrococcus dentrificans. II. The properties of pyridine nucleotide transhydrogenase. , 1967, Biochimica et biophysica acta.

[30]  A. H. Stouthamer,et al.  Utilization of energy for growth and maintenance in continuous and batch cultures of microorganisms. A reevaluation of the method for the determination of ATP production by measuring molar growth yields. , 1973, Biochimica et biophysica acta.

[31]  R. Sato,et al.  Oxidative phosphorylation in Micrococcus denitrificans. I. Preparation and properties of phosphorylating membrane fragments. , 1967, Biochimica et biophysica acta.

[32]  P. Garland,et al.  Respiration-driven proton translocation by yeast mitochondria with differing efficiencies of oxidative phosphorylation. , 1973, The Biochemical journal.

[33]  P. Mitchell,et al.  Proton translocation coupled to ATP hydrolysis in rat liver mitochondria. , 1968, European journal of biochemistry.

[34]  P. Garland,et al.  Non-haem iron and the dissociation of piericidin A sensitivity from site 1 energy conservation in mitochondria from Torulopsis utilis. , 1971, The Biochemical journal.

[35]  P. Garland,et al.  A comparison of mitochondria from Torulopsis utilis grown in continuous culture with glycerol, iron, ammonium, magnesium or phosphate as the growth-limiting nutrient. , 1971, The Biochemical journal.

[36]  P. Bragg,et al.  The effect of iron deficiency on respiration and energy-coupling in Escherichia coli. , 1973, Journal of general microbiology.

[37]  M. Doudoroff,et al.  Proposal to reject the genus Hydrogenomonas: Taxonomic implications , 1969 .

[38]  P. Mitchell,et al.  Respiration-driven proton translocation in micrococcus denitrificans , 1970, Journal of bioenergetics.

[39]  R. Poole,et al.  Effects of sulphate-limited growth in continuous culture on the electron-transport chain and energy conservation in Escherichia coli K12. , 1975, The Biochemical journal.

[40]  B. Seddon,et al.  Orthophosphate analysis by the Fiske-SubbaRow method and interference by adenosine phosphates and pyrophosphate at variable acid pH. , 1973, Analytical biochemistry.

[41]  F. R. Whatley,et al.  Oxidative phosphorylation coupled to oxygen uptake and nitrate reduction in Micrococcus denitrificans. , 1970, Biochimica et biophysica acta.

[42]  S. Pirt.  The maintenance energy of bacteria in growing cultures , 1965, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[43]  P. Garland,et al.  Proton translocation and the respiratory nitrate reductase of Escherichia coli. , 1975, The Biochemical journal.

[44]  D. Meyer,et al.  Oxidative phosphorylation in bacteria which contain different cytochrome oxidases. , 1973, European journal of biochemistry.

[45]  Portland Press Ltd.  Respiration-driven proton translocation in rat liver mitochondria , 1968 .

[46]  C. W. Jones,et al.  Respiration‐linked proton translocation in Azotobacter vinelandii , 1975, FEBS letters.

[47]  R. Sato,et al.  Oxidative phosphorylation in Micrococcus denitrificans. IV. Further characterization of electron-transfer pathway and phosphorylation activity in NADH oxidation. , 1968, Journal of biochemistry.

[48]  J. Chappell,et al.  Respiration-Driven Proton Translocation in Hydrogenomonas eutropha H-16 , 1974 .

[49]  A. H. Stouthamer,et al.  Determination of the efficiency of oxidative phosphorylation in continuous cultures of Aerobacter aerogenes , 1975, Archives of Microbiology.