Archives of Microbiology

, Volume 146, Issue 4, pp 396–401 | Cite as

Manganese deficiency impairs ribonucleotide reduction but not DNA replication in Arthrobacter species

  • J. Plönzig
  • G. Auling
Original Papers
Received:
Accepted:

Abstract

Manganese deficiency induced unbalanced growth, filamentous morphology and a decrease of viability in Arthrobacter citreus ATCC 11624, A. globiformis ATCC 8010 and A. oxydans DSM 420. Under these conditions whole cells showed an inhibition of DNA formation but not of RNA synthesis. However, DNA replication still functioned when manganese-deficient cells were made permeable to and supplied with all four deoxyribonucleotides. The inhibition of DNA formation in-vivo could be traced back to impairment of DNA precursor biosynthesis as ribonucleotide reductase activity was distinctly reduced upon starvation of manganese. Both DNA formation in-vivo and ribonucleotide reductase activity were restored in the starved cultures by addition of Mn2+ but not of other divalent cations. In these manganese-reactivated cultures both processes were stimulated above the levels of the manganese-sufficient controls. Rifampicin or chloramphenicol (both 100 μg/ml) could not suppress the rapid manganese-reactivation of cultures starved of this cation. This suggests the presence of an inactive metal-deficient ribonucleotide reductase apoenzyme in manganese-deficient cells. The presence of a manganese-dependent ribonucleotide reduction in the genus Arthrobacter besides of Brevibacterium ammoniagenes and Micrococcus luteus indicates a broad distribution of this new type of metal catalysis for DNA precursor biosynthesis in the high GC% branch of the Gram-positive bacteria.

Key words

Manganese-deficiency Decrease of viability Arthrobacter citreus Arthrobacter globiformis Arthrobacter oxydans Inhibition of DNA precursor biosynthesis Manganese-dependent ribonucleotide reduction Coryneform bacteria 

Abbreviations

HU

hydroxyurea

TCA

trichloroacetic acid

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References

  1. Archibald F (1986) Manganese: its acquisition by and function in the lactic acid bacteria. CRC Critical Rev Microbiol 13:63–109Google Scholar
  2. Auling G (1983) The effect of manganese limitation on DNA precursor biosynthesis during nucleotide fermentation with Brevibacterium ammoniagenes and Micrococcus luteus. Eur J Appl Microbiol Biotechnol 18:229–235Google Scholar
  3. Auling G, Thaler M, Diekmann H (1980) Parameters of unbalanced growth and reversible inhibition of deoxyribonucleic acid synthesis in Brevibacterium ammoniagenes ATCC 6872 induced by depletion of Mn2+. Inhibitor studies on the reversibility of deoxyribonucleic acid synthesis. Arch Microbiol 127:105–114Google Scholar
  4. Bhattacharya S, Sarkar N (1981) Study of deoxyribonucleic acid replication in permeable cells of Bacillus subtilis using mercurated nucleotide substrates. Biochemistry 20:3029–3034Google Scholar
  5. Carell EF, Seeger JW (1980) Ribonucleotide reductase activity in vitamin B12-deficient Euglena gracilis. Biochem J 188:573–576Google Scholar
  6. Cowles JR, Evans HJ, Russell SA (1969) B12 coenzyme-dependent ribonucleotide reductase in Rhizobium species and the effect of cobalt deficiency on the activity of the enzyme. J Bacteriol 97:1460–1465Google Scholar
  7. Davis BD, Mingioli ES (1950) Mutants of Escherichia coli requiring methionine or vitamin B12. J Bacteriol 60:17–28Google Scholar
  8. Eberwein H, Gries FA, Decker K (1961) Über den Abbau des Nicotins durch Bakterienenzyme. II. Isolierung und Charakterisierung eines nicotin-abbauenden Bodenbakteriums. Hoppe-Seyler's Z Physiol Chem 323:236–248Google Scholar
  9. Engström Y, Eriksson S, Thelander L, Akerman M (1979) Ribonucleotide reductase from calf thymus. Purification and properties. Biochemistry 18:2941–2948Google Scholar
  10. Fiedler F, Schleifer K, Kandler O (1973) Amino acid sequence of the threonine-containing mureins of coryneform bacteria. J Bacteriol 113:8–17Google Scholar
  11. Follmann H, Willing A, Auling G, Plönzig J (1986) Manganese and ribonucleotide reduction in Gram-positive bacteria. In: Holmgren A, Bränden C-I, Jörnvall H, Sjöberg B-M (eds) Thioredoxin and glutaredoxin systems: Structure and function. Raven Press, New York, pp 217–226Google Scholar
  12. Gleason FK, Hogenkamp HPC (1972) 5′-Deoxyadenosylcobalamin-dependent ribonucleotide reductase: a survey of its distribution. Biochim Biophys Acta 277:466–470Google Scholar
  13. Hammarsten E, Reichard P, Saluste E (1950) Pyrimidine nucleosides as precursors of pyrimidines in polynucleotides. J Biol Chem 183:105–109Google Scholar
  14. Hogenkamp HPC (1984) Nature and properties of the bacterial ribonucleotide reductases. Pharmac Ther 23:393–405Google Scholar
  15. Keddie RM, Jones D (1981) Saprophytic, aerobic coryneform bacteria. In: Starr MP, Stolp H, Trüper HG, Balows A, Schlegel HG (eds) The prokaryotes. Springer, Berlin Heidelberg New York, pp 1838–1878Google Scholar
  16. Lammers M, Follmann H (1983) The ribonucleotide reductases: A unique group of metalloenzymes essential for cell proliferation. Struct Bonding 54:27–91Google Scholar
  17. Ogata K, Kinoshita S, Tsunoda T, Aida K (1976) Microbial production of nucleic acid-related substances. Halsted Press, Kodansha Ltd, Tokyo; John Wiley & Sons Inc, New York London Sydney TorontoGoogle Scholar
  18. Oka T, Udagawa K, Kinoshita S (1968) Unbalanced growth death due to depletion of Mn2+ in Brevibacterium ammoniagenes. J Bacteriol 96:1760–1767Google Scholar
  19. Pal BC, Regan JD, Hamilton FD (1975) Separation of bases, ribonucleosides and deoxyribonucleotides by anion-exclusion and partition chromatography on cation-exchange resin: application to the assay of ribonucleotide reductase, deaminase and nucleosidase. Anal Biochem 67:625–633Google Scholar
  20. Scherer CG, Boylen CW (1977) Macromolecular synthesis and degradation in Arthrobacter during periods of nutrient deprivation. J Bacteriol 132:584–589Google Scholar
  21. Schimpff-Weiland G, Follmann H, Auling G (1981) A new manganese-activated ribonucleotide reductase found in Gram-positive bacteria. Biochem Biophys Res Commun 102:1276–1282Google Scholar
  22. Stackebrandt E, Fiedler F (1979) DNA-DNA homology studies among strains of Arthrobacter and Brevibacterium. Arch Microbiol 120:289–295Google Scholar
  23. Stackebrandt E, Lewis BJ, Woese CR (1980) The phylogenetic structure of the coryneform group of bacteria. Zbl Bakt Hyg, I Abt Orig C1:137–149Google Scholar
  24. Stackebrandt E, Fowler CJ, Fiedler F, Seiler H (1983) Taxonomic studies on Arthrobacter nicotianae and related taxa: description of Arthrobacter uratoxydans sp. nov. and Arthrobacter sulfureus sp. nov. and reclassification of Brevibacterium protophormiae as Arthrobacter protophormiae comb. nov. System Appl Microbiol 4:470–486Google Scholar
  25. Thaler M, Diekmann H (1979) The effect of manganese deficiency in lipid content and composition in Brevibacterium ammoniagenes. Eur J Appl Microbiol Biotechnol 6:379–387Google Scholar
  26. Thelander L, Reichard P (1979) Reduction of ribonucleotides. Ann Rev Biochem 48:133–158Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • J. Plönzig
    • 1
  • G. Auling
    • 1
  1. 1.Institut für MikrobiologieUniversität HannoverHannover 1Germany

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