Skip to main content
Log in

Presence of oxygen-consuming ribonucleotide reductase in corrinoid-deficientPropionibacterium freudenreichii

  • Short Communication
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Corrinoid-deficientPropionibacterium freudenreichii subsp. shermanii showed adenosylcobalamin-(AdoCb1)-independent ribonucleotide reductase (RNR) activity in the presence of air. Increasing the incubation time with free access of O2 led to an increase in RNR activity. As polarographic estiamtions of O2 uptake demonstrated, AdoCb1-independent RNR activity (with ADP as substrate) in a cell-free system of corrinoid-deficientP. freudenreichii was accompanied by specific molecular oxygen consumption. The activity was not inhibited by carbonyl cyanidem-chlorophenylhydrazone (CCCP) or carbonyl cyanidep-(trifluoromethoxy)phenylhydrazone (FCCCP). The activity was present in the cytoplasmic membrane-free soluble fraction of the cell extract, and it was inhibited by hydroxyurea. Manganese ions were important for the cell division of corrinoid-deficientP. freudenreichii and stimulated RNR activity after 8-hydroxyquinoline or EDTA treatment of the cell extract. We therefore concluded thatP. freudenreichii is able to form DNA (deoxyribosylic precursors) using AdoCb1-dependent ribonucleotide reductase and also with an alternative AdoCb1-independent molecular-oxygen-consuming RNR system.

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.

Institutional subscriptions

References

  • Auling G, Follmann H (1994) Manganese-dependent ribonucleotide reduction and overproduction of nucleotides in coryneform bacteria. In: Siegel H, Siegel A (eds) Metal ions in biological systems, vol 30. Dekker, New York London Basel Hong Kong, pp 131–161

    Google Scholar 

  • Ashley GW, Stubbe J (1985) Current ideas on the chemical mechanism of ribonucleotide reductases. Pharmacol Ther 30:301–329

    Article  PubMed  CAS  Google Scholar 

  • Barlow T, Eliasson R, Platz A, Reichard P, Sjöberg B-M (1983) Enzymatic modification of tyrosine to a stable free radical in ribonucleotide reductase. Proc Natl Acad Sci USA 80:1492–1495

    Article  PubMed  CAS  Google Scholar 

  • Bergey’s manual of determinative bacteriology, 9th edn (1994) Holt JG, Sneath PHA, Staley JT, Krieg NR, Williams ST (eds). Williams and Wilkins, Baltimore, pp 571–596

    Google Scholar 

  • Blakley RL (1978) Ribonucleoside triphosphate reductase fromLactobacillus leichmanii. Methods Enzymol 51:246–259

    PubMed  CAS  Google Scholar 

  • Bryukhacheva NL, Bonartseva GA, Vorob’ova LI (1975) Oxidative phosphorylation in propionic acid bacteria. Mikrobiologiya 44:11–15

    CAS  Google Scholar 

  • Cory JG (1988) Ribonucleotide reductase as a chemotherapeutic target. In: Weber G (ed) Advances in enzyme regulation, vol 27. Pergamon Press, Oxford New York, pp 449–453

    Google Scholar 

  • Daniels L, Hanson RS, Phillips JA (1994) Chemical analysis. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington DC, pp 542–544

    Google Scholar 

  • Eliasson R, Jörnvall H, Reichard P (1986) Superoxide dismutase participates in the enzymatic formation of the tyrosine radical of ribonucleotide reductase fromEscherichia coli. Proc Natl Acad Sci USA 83:2373–2377

    Article  PubMed  CAS  Google Scholar 

  • Follmann H (1982) Deoxyribonucleotide synthesis and the emergence of DNA in molecular evolution. Naturwissenschaften 69: 75–81

    Article  PubMed  CAS  Google Scholar 

  • Follmann H, Harder J (1989) The different types of ribonucleotide reductase in unicellular eukaryotes and bacteria: a comparative view. In: Kotyka A, Škoda J, Pačes V, Kostka V (eds) Highlights of modern biochemistry. Proceedings of the 14th International Congress Biochemistry, Prague 10–15 July 1988, vol 1. Utrecht, Tokyo, pp 203–214

  • Fontecave M, Eliasson R, Reichard P (1989) Oxygen-sensitive ribonucleotide triphosphate reductase is present in anaerobicEscherichia coli. Proc Natl Acad Sci USA 86:2147–2151

    Article  PubMed  CAS  Google Scholar 

  • Harder J (1993) Ribonucleotide reductases and their occurrence in microorganisms: a link to the RNA/DNA transition. FEMS Microbiol Rev 12:273–292

    Article  PubMed  CAS  Google Scholar 

  • Hockertz S, Plönzig J, Auling G (1987) Impairment of DNA formation is an early event inAspergillus niger under manganese starvation. Appl Microbiol Biotechnol 25:590–593

    Article  CAS  Google Scholar 

  • Hogenkamp HPC, Follmann H, Thauer RK (1987) Ribonucleotide reductase in cell extracts ofMethanobacterium thermoautotrophicum. FEBS Lett 219:197–201

    Article  CAS  Google Scholar 

  • Holmgren A (1981) Regulation of ribonucleotide reductase. In: Horecker BL, Stadtman ER (eds) Current topics in cell regulation, vol 19. Academic Press, New York London, pp 47–76

    Google Scholar 

  • Iordan EP (1990) Vitamin B12 in DNA formation of microorganisms (review). Usp Sovremennoy Biol 110:79–89

    Google Scholar 

  • Iordan EP (1992) Modulation in DNA formation ofPropionibacterium freudenreichii subsp. shermanii under conditions of corrinoid limitation. Mikrobiologiya 61:341–346

    CAS  Google Scholar 

  • Iordan EP, Petukhova NI (1989) Reorganization of the ribonucleotide reductase system in propionic acid bacteria with inhibited synthesis of vitamin B12. Mikrobiologiya 58:533–538

    CAS  Google Scholar 

  • Iordan EP, Pryanishnikova NI (1994) Intensification ofPropionibacterium freudenreichii DNA formation by 5,6-dimethylbenzimidasole. Prikl Biokhim Mikrobiol 30:137–142

    CAS  Google Scholar 

  • Iordan EP, Vorob’ova LI, Gaitan VI (1975) Ribonucleotide reductase ofPropionibacterium shermanii. Mikrobiologiya 44:609–614

    CAS  Google Scholar 

  • Koller CA, Stetson PL, Nichamin LD, Mitchell BS (1980) An assay of deoxyadenosine and adenosine in human plasma by HPLC. Biochem Med 24:179–184

    Article  PubMed  CAS  Google Scholar 

  • Lammers M, Follmann H (1983) The ribonucleotide reductases—a unique group of metalloenzymes essential for cell proliferation. Structure Bond 54:27–91

    Article  CAS  Google Scholar 

  • Plönzig J, Auling G (1987) Manganese deficiency impairs ribonucleotide reduction but not DNA replication inArthrobacter species. Arch Microbiol 146:396–401

    Article  Google Scholar 

  • Probst H, Schiffer H, Gekeler V, Scheffler K (1989) Oxygen-dependent regulation of mammalian ribonucleotide reductase in vivo and possible signification for replication initiation. Biochem Biophys Res Commun 163:334–340

    Article  PubMed  CAS  Google Scholar 

  • Reichard P (1985) Ribonucleotide reductase and deoxyribonuleotide pools. In: Genetic consequences of nucleotide pool imbalance. Proceedings of Conference, Research Triangle Park, NC, May 9–11 1983, New York London, pp 33–45

  • Reichard P (1993a) From RNA to DNA, why so many ribonucleotide reductases. Science 260:1773–1777

    Article  PubMed  CAS  Google Scholar 

  • Reichard P (1993b) The anaerobic ribonucleotide reductase fromEscherichia coli. J Biol Chem 268:8383–8386

    PubMed  CAS  Google Scholar 

  • Schimpff-Weiland G, Follmann H, Auling G (1981) A new manganese activated ribonucleotide reductase found in gram-positive bacteria. Biochem Biophys Res Commun 102:1276–1282

    Article  PubMed  CAS  Google Scholar 

  • Schwartz AC, Sporkenbach J (1975) The electron transport system of the anaerobicPropionibacterium shermanii. Cytochrome and inhibitor studies. Arch Microbiol 102:261–273

    Article  PubMed  CAS  Google Scholar 

  • Sone N (1972) The redox reactions in propionic acid fermentation. I. Occurrence and nature of an electron transfer system inPropionibacterium arabinosum. J Biochem 71:931–940

    PubMed  CAS  Google Scholar 

  • Stackebrandt E, Woese CR (1981) Towards a phylogeny of actinomyces and related organisms. Curr Microbiol 5:131–136

    Article  Google Scholar 

  • Stubbe JA (1985) Mechanism of B12-dependent ribonucleotide reductase. Mol Cell Biochem 50:25–45

    Google Scholar 

  • Sze I S-J, McFarlan SC, Spormann A, Hogenkamp HPC, Follmann H (1992) A possible new class of ribonucleotide reductase fromMethanobacterium thermoautotrophicum. Biochem Biophys Res Commun 184:1101–1107

    Article  PubMed  CAS  Google Scholar 

  • Thelander L, Gräslund A, Thelander M (1983) Continual presence of oxygen and iron required for mammalian ribonucleotide reduction: possible regulation mechanism. Biochem Biopys Res Commun 110:859–865

    Article  CAS  Google Scholar 

  • Vorob’ova LI, Kraeva NI (1982) Superoxide radicals and antiradical defence of propionic acid bacteria. Arch Microbiol 133: 110–113

    Article  Google Scholar 

  • Willing A, Follmann H, Auling G (1988) Nucleotide and thioredoxin specificity of the manganese ribonucleotide reductase fromBrevibacterium ammoniagenes. Eur J Biochem 175:167–173

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Iordan, E.P., Petukhova, N.I. Presence of oxygen-consuming ribonucleotide reductase in corrinoid-deficientPropionibacterium freudenreichii . Arch. Microbiol. 164, 377–381 (1995). https://doi.org/10.1007/BF02529986

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02529986

Key words

Navigation