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Current views on the regulation of autotrophic carbon dioxide fixation via the Calvin cycle in bacteria

  • Physiology And Growth
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Abstract

The Calvin cycle of carbon dioxide fixation constitutes a biosynthetic pathway for the generation of (multi-carbon) intermediates of central metabolism from the one-carbon compound carbon dioxide. The product of this cycle can be used as a precursor for the synthesis of all components of cell material. Autotrophic carbon dioxide fixation is energetically expensive and it is therefore not surprising that in the various groups of autotrophic bacteria the operation of the cycle is under strict metabolic control. Synthesis of phosphoribulokinase and ribulose-1,5-bisphosphate carboxylase, the two enzymes specifically involved in the Calvin cycle, is regulated via end-product repression. In this control phosphoenolpyruvate most likely has an alarmone function. Studies of the enzymes isolated from various sources have indicated that phosphoribulokinase is the target enzyme for the control of the rate of carbon dioxide fixation via the Calvin cycle through modulation of existing enzyme activity. In general, this enzyme is strongly activated by NADH, whereas AMP and phosphoenol-pyruvate are effective inhibitors. Recent studies of phosphoribulokinase inAlcaligenes eutrophus suggest that this enzyme may also be regulated via covalent modification.

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References

  • Andersen, K. 1979. Mutations altering the catalytic activity of a plant-type ribulose bisphosphate carboxylase/oxygenase inAlcaligenes eutrophus. — Biochim. Biophys. Acta585: 1–11.

    CAS  PubMed  Google Scholar 

  • Beudeker, R. F. 1981. Obligate chemolithotrophy: its ecophysiological implications forThiobacillus neapolitanus. — Ph. D. Thesis, University of Groningen.

  • Beudeker, R. F., Cannon, G. C., Kuenen, J. G. andShively, J. M. 1980. Relations betweend-ribulose-1,5-bisphosphate carboxylase, carboxysomes and CO2 fixing capacity in the obligate chemolithotrophThiobacillus neapolitanus grown under different limitations in the chemostat. — Arch. Microbiol.124: 185–189.

    Article  CAS  Google Scholar 

  • Bowien, L. andLeadbeater, L. 1984. Molecular and cellular regulation of carbon dioxide assimilation in bacteria. p. 9–13.In R. L. Crawford and R. S. Hanson (eds), Microbial Growth on C1 Compounds. — American Society for Microbiology, Washington, D.C.

    Google Scholar 

  • Calvin, M. 1962. The path of carbon in photosynthesis. — Science135: 879–889.

    CAS  PubMed  Google Scholar 

  • Cohen, Y., De Jonge, I. andKuenen, J. G. 1979. Excretion of glycolate byThiobacillus neapolitanus grown in continuous culture. — Arch. Microbiol.122: 189–194.

    Article  CAS  Google Scholar 

  • Curtis, S. E. andHaselkorn, R. 1983. Isolation and sequence of the gene for the large subunit of ribulose-1,5-bisphosphate carboxylase from the cyanobacteriumAnabaena 7120. — Proc. Natl Acad. Sci. USA80: 1835–1839.

    CAS  PubMed  Google Scholar 

  • Dijkhuizen, L. 1979. Regulation of autotrophic and heterotrophic metabolism inPseudomonas oxalaticus OX1. — Ph. D. Thesis, University of Groningen.

  • Dijkhuizen, L. andHarder, W. 1979a. Regulation of autotrophic and heterotrophic metabolism inPseudomonas oxalaticus OX1: growth on mixtures of acetate and formate in continuous culture. — Arch. Microbiol.123: 47–53.

    CAS  Google Scholar 

  • Dijkhuizen, L. andHarder, W. 1979b. Regulation of autotrophic and heterotrophic metabolism inPseudomonas oxalaticus OX1: growth on mixtures of oxalate and formate in continuous culture. — Arch. Microbiol.123: 55–63.

    CAS  Google Scholar 

  • Dijkhuizen, L. andHarder, W. 1984. Regulation of autotrophic and heterotrophic metabolism inPseudomonas oxalaticus OX1. Growth on fructose and on mixtures of fructose and formate in batch and continuous cultures. — J. Gen. Microbiol.130: 447–457.

    CAS  Google Scholar 

  • Dijkhuizen, L. andHarder, W. 1985. Microbial metabolism of carbon dioxide.In H. Dalton (ed.), Comprehensive Biotechnology, Vol. 1, The Principles of Biotechnology. — Pergamon Press Ltd, Oxford (in press).

    Google Scholar 

  • Dijkhuizen, L., Knight, M. andHarder W. 1978. Metabolic regulation inPseudomonas oxalaticus OX1. Autotrophic and heterotrophic growth on mixed substrates. — Arch. Microbiol.116: 77–83.

    Article  CAS  PubMed  Google Scholar 

  • Ellis, R. J. 1979. The most abundant protein in the world. — Trends Biochem. Sci.4: 241–244.

    Article  CAS  Google Scholar 

  • Evans, M. C. W., Buchanan, B. B. andArnon, D. I. 1966. A new ferredoxin-dependent carbon reduction cycle in a photosynthetic bacterium. — Proc. Natl Acad. Sci. USA55: 928–934.

    CAS  PubMed  Google Scholar 

  • Flügge, U. I., Stitt, M., Freisl, M. andHeldt, H. W. 1982. On the participation of phosphoribulokinase in the light regulation of CO2 fixation. — Plant Physiol.69: 263–267.

    Google Scholar 

  • Friedrich, C. G. 1982. Derepression of hydrogenase during limitation of electron donors and derepression of ribulosebisphosphate carboxylase during carbon limitation ofAlcaligenes eutrophus. — J. Bacteriol.149: 203–210.

    CAS  PubMed  Google Scholar 

  • Friedrich, C. G., Friedrich, B. andBowien, B. 1981. Formation of enzymes of autotrophic metabolism during heterotrophic growth ofAlcaligenes eutrophus. — J. Gen. Microbiol.122: 69–78.

    CAS  Google Scholar 

  • Fuchs, G. andStupperich, E. 1984. CO2 reduction to cell carbon in methanogens. p. 199–202.In R. L. Crawford and R. S. Hanson (eds), Microbial Growth on C1 Compounds. — American Society for Microbiology, Washington, D. C.

    Google Scholar 

  • Gibson, J. L. andTabita, F. R. 1977. Different molecular forms ofd-ribulose-1,5-bisphosphate carboxylase fromRhodopseudomonas sphaeroides. — J. Biol. Chem.252: 943–949.

    CAS  PubMed  Google Scholar 

  • Gibson, J. L. andTabita, F. R. 1979. Activation of ribulose 1,5-bisphosphate carboxylase fromRhodopseudomonas sphaeroides: probable role of the small subunit. — J. Bacteriol.140: 1023–1027.

    CAS  PubMed  Google Scholar 

  • Gottschal, J. C. andKuenen, J. G. 1980. Mixotrophic growth ofThiobacillus A2 on acetate and thiosulfate as growth limiting substrates in the chemostat. — Arch. Microbiol.126: 33–42.

    Article  CAS  Google Scholar 

  • Hart, B. A. andGibson, J. 1971. Ribulose-5-phosphate kinase fromChromatium sp. strain D. — Arch. Biochem. Biophys.144: 308–321.

    Article  CAS  PubMed  Google Scholar 

  • Herbert, D., Elsworth, R. andTelling, R. C. 1956. The continuous culture of bacteria; a theoretical and experimental study. — J. Gen. Microbiol.14: 601–622.

    CAS  PubMed  Google Scholar 

  • Im, D.-S. andFriedrich, C. G. 1983. Fluoride, hydrogen, and formate activate ribulosebisphosphate carboxylase formation inAlcaligenes eutrophus. — J. Bacteriol.154: 803–808.

    CAS  PubMed  Google Scholar 

  • Karagouni, A. D. andSlater, J. H. 1979. Enzymes of the Calvin cycle and intermediary metabolism in the cyanobacteriumAnacystis nidulans grown in chemostat cultures. — J. Gen. Microbiol.115: 369–376.

    CAS  Google Scholar 

  • Kiesow, L. A., Lindsley, B. F. andBless, J. W. 1977. Phosphoribulokinase fromNitrobacter winogradskyi: activation by reduced nicotinamide adenine dinucleotide and inhibition by pyridoxal phosphate. — J. Bacteriol.130: 20–25.

    CAS  PubMed  Google Scholar 

  • Kuenen, J. G. andVeldkamp, H. 1973. Effects of organic compounds on growth of chemostat cultures ofThiomicrospira pelophila, Thiobacillus thioparus andThiobacillus neapolitanus. — Arch. Mikrobiol.94: 173–190.

    Article  CAS  PubMed  Google Scholar 

  • Leadbeater, L. andBowien, B. 1984. Control of autotrophic carbon assimilation inAlcaligenes eutrophus by inactivation and reactivation of phosphoribulokinase. — J. Bacteriol.157: 95–99.

    CAS  PubMed  Google Scholar 

  • Leadbeater, L., Siebert, K., Schobert, P. andBowien, B. 1982. Relationship between activities and protein levels of ribulosebisphosphate carboxylase and phosphoribulokinase inAlcaligenes eutrophus. — FEMS Microbiol. Lett.14: 263–266.

    CAS  Google Scholar 

  • Lorimer, G. H., Badger, M. R. andAndrews, T. J. 1976. The activation of ribulose-1,5-bisphosphate carboxylase by carbon dioxide and magnesium ions. Equilibria, kinetics, a suggested mechanism, and physiological implications. — Biochemistry15: 529–536.

    Article  CAS  PubMed  Google Scholar 

  • MacElroy, R. D., Johnson, E. J. andJohnson, M. K. 1969. Control of ATP-dependent CO2 fixation in extracts ofHydrogenomonas facilis: NADH regulation of phosphoribulokinase. — Arch. Biochem. Biophys.131: 272–275.

    Article  CAS  PubMed  Google Scholar 

  • MacElroy, R. D., Mack, H. M. andJohnson, E. J. 1972. Properties of phosphoribulokinase fromThiobacillus neapolitanus. — J. Bacteriol.112: 532–538.

    CAS  PubMed  Google Scholar 

  • Marsden, W. J. N. andCodd, G. A. 1984. Purification and molecular and catalytic properties of phosphoribulokinase from the cyanobacteriumChlorogloeopsis fritschii. — J. Gen. Microbiol.130: 999–1006.

    CAS  Google Scholar 

  • McFadden, B. A. andTabita, F. R. 1974.d-Ribulose-1,5-diphosphate carboxylase and the evolution of autotrophy. — Biosystems6: 93–112.

    Article  CAS  PubMed  Google Scholar 

  • Miziorko, H. M. andLorimer, G. H. 1983. Ribulose-1,5-bisphosphate carboxylase-oxygenase. — Annu. Rev. Biochem.52: 507–535.

    Article  CAS  PubMed  Google Scholar 

  • Ogren, W. L. 1984. Photorespiration: pathways, regulation, and modification. — Annu. Rev. Plant Physiol.35: 415–442.

    Article  CAS  Google Scholar 

  • Ohmann, E. 1979. Autotrophic carbon dioxide assimilation in prokaryotic microorganisms. p. 54–67.In A. Pirson and M. H. Zimmermann (eds), Encyclopedia of Plant Physiology, Vol. 6, Photosynthesis II. — Springer Verlag, Berlin.

    Google Scholar 

  • Reutz, I., Schobert, P. andBowien, B. 1982. Effect of phosphoglycerate mutase deficiency on heterotrophic and autotrophic carbon metabolism ofAlcaligenes eutrophus. — J. Bacteriol.151: 8–14.

    CAS  PubMed  Google Scholar 

  • Rittenberg, S. C. 1969. The roles of exogenous organic matter in the physiology of chemolithotrophic bacteria. — Adv. Microb. Physiol.3: 159–196.

    CAS  Google Scholar 

  • Sani, A., De Koning, W., Dijkhuizen, L. andDow, C. S. 1983. Studies on the ribulose-1,5-bisphosphate carboxylase from the Rhodospirillaceae. — Proc. 4th Int. Symp. Microbial Growth on C1 Compounds, Minneapolis, U.S.A., p. 312.

  • Sarles, L. S. andTabita, F. R. 1983. Derepression of the synthesis ofd-ribulose 1,5-bisphosphate carboxylase/oxygenase fromRhodospirillum rubrum. — J. Bacteriol.153: 458–464.

    CAS  PubMed  Google Scholar 

  • Shinozaki, K., Yamada, C., Takahata, N. andSugiura, M. 1983. Molecular cloning and sequence analysis of the cyanobacterial gene for the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. — Proc. Natl Acad. Sci. USA80: 4050–4054.

    CAS  PubMed  Google Scholar 

  • Siebert, K., Schobert, P. andBowien, B. 1981. Purification, some catalytic and molecular properties of phosphoribulokinase fromAlcaligenes eutrophus. — Biochim. Biophys. Acta658: 35–44.

    CAS  PubMed  Google Scholar 

  • Slater, J. H. andMorris, I. 1973. Photosynthetic carbon dioxide assimilation byRhodospirillum rubrum. — Arch. Mikrobiol.88: 213–223.

    Article  CAS  PubMed  Google Scholar 

  • Smith, A. J. andHoare, D. S. 1977. Specialist phototrophs, lithotrophs, and methylotrophs: a unity among a diversity of procaryotes? — Bacteriol. Rev.41: 419–448.

    CAS  PubMed  Google Scholar 

  • Somerville, C. R. andSomerville, S. C. 1984. Cloning and expression of theRhodospirillum rubrum ribulosebisphosphate carboxylase gene inE. coli. — Mol. Gen. Genet.193: 214–219.

    Article  CAS  Google Scholar 

  • Srivastava, S., Urban, M. andFriedrich, B. 1982. Mutagenesis ofAlcaligenes eutrophus by insertion of the drug-resistance transposon Tn5. — Arch. Microbiol.131: 203–207.

    Article  CAS  PubMed  Google Scholar 

  • Storrø, I. andMcFadden, B. A. 1981. Glycolate excretion byRhodospirillum rubrum. — Arch. Microbiol.129: 317–320.

    Article  Google Scholar 

  • Tabita, F. R. 1980. Pyridine nucleotide control and subunit structure of phosphoribulokinase from photosynthetic bacteria. — J. Bacteriol.143: 1275–1280.

    CAS  PubMed  Google Scholar 

  • Tabita, F. R. 1981. Molecular regulation of carbon dioxide assimilation in autotrophic microorganisms. p. 70–82.In H. Dalton (ed.), Microbial Growth on C1 Compounds. — Heyden and Son, London.

    Google Scholar 

  • Tabita, F. R., Martin, M. N., Beudeker, R. F., Quivey Jr, R. G., Sarles, L. S. andWeaver, K. E. 1984. Control of carbon dioxide fixation. p. 3–8.In R. L. Crawford and R. S. Hanson (eds), Microbial Growth on C1 Compounds. — American Society for Microbiology, Washington, D.C.

    Google Scholar 

  • Tabita, F. R. andMcFadden, B. A. 1974.d-Ribulose 1,5-diphosphate carboxylase fromRhodospirillum rubrum. II. Quaternary structure, composition, catalytic, and immunological properties. — J. Biol. Chem.249: 3459–3464.

    CAS  PubMed  Google Scholar 

  • Tabita, F. R., Sarles, L. S., Quivey Jr, R. G., Weaver, K. E. andWaddill, F. E. 1983. Molecular regulation, mechanism and enzymology of autotrophic carbon dioxide fixation. p. 148–154.In D. Schlessinger (ed.), Microbiology-1983. — American Society for Microbiology, Washington, D. C.

    Google Scholar 

  • Van Verseveld, H. W., Boon, J. P. andStouthamer, A. H. 1979. Growth yields and the efficiency of oxidative phosphorylation ofParacoccus denitrificans during two-(carbon) substrate-limited growth. — Arch. Microbiol.121: 213–223.

    Article  Google Scholar 

  • Weaver, K. E. andTabita, F. R. 1983. Isolation and partial characterization ofRhodopseudomonas sphaeroides mutants defective in the regulation of ribulose bisphosphate carboxylase/oxygenase. — J. Bacteriol.156: 507–515.

    CAS  PubMed  Google Scholar 

  • Whitman, W. B., Martin, M. N. andTabita, F. R. 1979. Activation and regulation of ribulose bisphosphate carboxylase-oxygenase in the absence of small subunits. — J. Biol. Chem.254: 10184–10189.

    CAS  PubMed  Google Scholar 

  • Wildner, G. F. 1981. Ribulose-1,5-bisphosphate carboxylase-oxygenase: aspects and prospects. — Physiol. Plant.52: 385–389.

    CAS  Google Scholar 

  • Zeikus, J. G. 1983. Metabolism of one-carbon compounds by chemotrophic anaerobes. — Adv. Microb. Physiol.24: 215–299.

    CAS  PubMed  Google Scholar 

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  1. Department of Microbiology, University of Groningen, Kerklaan 30, 9751 NN, Haren, The Netherlands

    L. Dijkhuizen & W. Harder

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  1. L. Dijkhuizen
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  2. W. Harder
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Dijkhuizen, L., Harder, W. Current views on the regulation of autotrophic carbon dioxide fixation via the Calvin cycle in bacteria. Antonie van Leeuwenhoek 50, 473–487 (1984). https://doi.org/10.1007/BF02386221

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