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Molecular Biology

, Volume 39, Issue 4, pp 482–494 | Cite as

Specific Features of Metabolism and Functions of High-Molecular Inorganic Polyphosphates in Yeasts as Representatives of Lower Eukaryotes

  • I. S. Kulaev
  • V. M. Vagabov
  • T. V. Kulakovskaya
  • N. A. Andreeva
  • L. P. Lichko
  • L. V. Trilisenko
Review and Experimantal Articles

Abstract

This review considers recent data demonstrating an important role of high-molecular-weight inorganic polyphosphates (polyPs) in regulatory processes in yeasts. PolyPs occur in various compartments of the cell and are metabolized by compartment-specific sets of enzymes. Evidence is provided for the multiplicity of polyP functions in the cells. Data on the pleiotropic effects of mutations of genes coding for polyP-metabolizing enzymes are summarized.

Key words

inorganic polyphosphate exopolyphosphatase endopolyphosphatase metabolism yeast 

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REFERENCES

  1. 1.
    Lieberman L. 1888. Uber das Nuclein der Hefe und kunstliche Darstellung eines Nucleus Eiweiss und Meta-phosphatsaure. Ber. Chem. Ges. 21, 598–607.Google Scholar
  2. 2.
    Bukhovich E, Belozersky A.N. 1958. Some aspects of polyphosphate formation in yeast cells. Biokhimiya. 23, 254–259.Google Scholar
  3. 3.
    Kulaev I.S., Belozersky A.N. 1962. Condensed inorganic phosphates in metabolism: 1. Izv. Akad. Nauk SSSR. 3, 354–368.Google Scholar
  4. 4.
    Liss E., Langen P. 1962. Versuche zur Polyphosphat-Uberkompensation in Heffenzellen nach Phosphatverarmung. Arch. Microbiol. 41, 383–392.Google Scholar
  5. 5.
    Harold F.M. 1966. Inorganic polyphosphates in biology: structure, metabolism, and functions. Bacteriol. Rev. 30, 772–794.PubMedGoogle Scholar
  6. 6.
    Kulaev I.S. 1975. Biokhimiya neorganicheskikh polifosfatov (Biochemistry of Inorganic Polyphosphates). Moscow: Izd. Mosk. Gos. Univ.Google Scholar
  7. 7.
    Kulaev I.S. 1979. The Biochemistry of Inorganic Polyphosphates. Wiley.Google Scholar
  8. 8.
    Kulaev I.S., Vagabov V.M. 1983. Polyphosphate metabolism in microorganisms. Adv. Microbiol. Physiol. 24, 83–171.Google Scholar
  9. 9.
    Wood H.G., Clark J.E. 1988. Biological aspects of inorganic polyphosphates. Ann. Rev. Biochem. 57, 235–260.CrossRefPubMedGoogle Scholar
  10. 10.
    Kornberg A. 1995. Inorganic polyphosphate: Toward making a forgotten polymer unforgettable. J. Bacteriol. 177, 491–496.PubMedGoogle Scholar
  11. 11.
    Kornberg A., Rao N.N., Ault-Riche D. 1999. Inorganic Polyphosphate: a molecule with many functions. Ann. Rev. Biochem. 68, 89–125.CrossRefPubMedGoogle Scholar
  12. 12.
    Kulaev I., Vagabov V., Kulakovskaya T. 1999. New aspects of polyphosphate metabolism and function. J. Biosci. Bioeng. 88, 111–129.CrossRefGoogle Scholar
  13. 13.
    Kulaev I.S., Kulakovskaya T.V. 2000. Polyphosphate and phosphate pump. Ann. Rev. Microbiol. 54, 709–735.CrossRefGoogle Scholar
  14. 14.
    Kulaev I., Vagabov V., Kulakovskaya T. 2004. The Biochemistry of Inorganic Polyphosphates, 2nd ed. Wiley.Google Scholar
  15. 15.
    Belozersky A.N. 1945. On the chemical nature of volutin. Mikrobiologiya. 14, 29–33.Google Scholar
  16. 16.
    Wiame J.M. 1947. Etude d’une substance polyphosphoree, basophillie et metachromatique chez les levures. Biochim. Biophys. Acta. 1. 234–255.CrossRefGoogle Scholar
  17. 17.
    Jacobson L., Helman M., Yariv J. 1982. The molecular composition of the volutin granules of yeast. Biochem. J. 201, 437–479.Google Scholar
  18. 18.
    Okorokov L.A., Lichko L.P., Kulaev I.S. 1980. Vacuoles: The main compartment of potassium, magnesium and phosphate ions in Saccharomyces carlsbergensis cells. J. Bacteriol. 144, 661–665.PubMedGoogle Scholar
  19. 19.
    Trilisenko L.V., Vagabov V.M., Kulaev I.S. 2002. Polyphosphate content and chain length in vacuoles of yeast Sannharimonas naravisiaa AEI Y-1173. Biokhimiya. 67, 592–596.Google Scholar
  20. 20.
    Reusch R.N., Sadoff H.L. 1988. Putative structure and functions of poly-beta-hydroxybutirate/calcium polyphosphate channel in bacterial plasma membranes. Proc. Natl. Acad. Sci. USA. 85, 4176–4180.PubMedGoogle Scholar
  21. 21.
    Rosh R. 2000. Transmembrane ion transport by polyphosphate-poly-(β)-hydroxybutyrate complexes. Biokhimiya. 65, 335–353.Google Scholar
  22. 22.
    Tijssen J.P.F., Beekes H.W., van Steveninck J. 1982. Localization of polyphosphate in Saccharomyces fragilis, as revealed by 4′,6′-diamidino-2-phenylindole fluorescence. Biochim. Biophys. Acta. 721, 394–398.CrossRefPubMedGoogle Scholar
  23. 23.
    Vagabov V.M., Chemodanova O.V., Kulaev I.S. Effect of inorganic polyphosphates on the magnitude of the electric charge of cell wall in yeast. Dokl. Akad. Nauk SSSR. 313, 989–992.Google Scholar
  24. 24.
    Tijssen J.P.F., Dubbelman T.M.A.R., van Steveninck J. 1983. Isolation and characterization of polyphosphates from the yeast cell surface. Biochim. Biophys. Acta. 760, 143–148.PubMedGoogle Scholar
  25. 25.
    Tijssen, J.P.F., van Steveninck J. 1984. Detection of a yeast polyphosphate fraction localized outside the plasma membrane by the method of phosphorus-31 nuclear magnetic resonance. Biochem. Biophys. Res. Commun. 119, 447–451.CrossRefPubMedGoogle Scholar
  26. 26.
    Tijssen J.P.F., van Steveninck J. 1985. Cytochemical staining of a yeast polyphosphate fraction, localized outside the plasma membrane. Protoplasma. 125, 124–128.CrossRefGoogle Scholar
  27. 27.
    Vorisek J., Knotkova A., Kotyk A. 1982. Fine cytochemical localization of polyphosphates in the yeast Saccharomyces cerevisiae. Zbl. Mikrobiol. 137, 421–432.Google Scholar
  28. 28.
    Vagabov V.M. 1988. Biosintez uglevodnykh komponentov kletochnoi stenki u drozzhei (Biosynthesis of Cell Wall Carbohydrates in Yeast). Pushchino: ONTI NTsBI.Google Scholar
  29. 29.
    Ivanov A.Yu., Vagabov V.M., Fomchenkov V.M., Kulaev I.S. 1996. Effect of cell wall polyphosphates on sensitivity to the damaging effect of cetyltrimethylammonium bromide in the yeast Sannharimonas narlsbargansis. Mikrobiologiya. 65, 611–616.Google Scholar
  30. 30.
    Shabalin Yu.A., Vagabov V.M., Kulaev I.S. 1978. Biosynthesis of high-molecular-weight polyphosphates from GDP-(P-32)-mannose by the membrane fraction of the yeast Sannharimonas narlsbargansis. Dokl. Akad. Nauk SSSR. 239, 490–492.Google Scholar
  31. 31.
    Shabalin Yu.A., Vagabov V.M., Kulaev I.S. 1979. On the mechanism of coupled biosynthesis of high-molecular-weight polyphosphates and mannan in the yeast Saccharomyces carlsbergensis. Dokl. Akad. Nauk SSSR. 249, 243–246.Google Scholar
  32. 32.
    Shabalin Yu.A., Kulaev I.S. 1989. Solubilization and properties of yeast dolichyldiphosphate: polyphosphate phosphotrasnferase. Biokhimiya. 54, 68–75.Google Scholar
  33. 33.
    Matile P.1978. Biochemistry and function of vacuoles. Ann. Rev. Plant Physiol. 29, 193–213.Google Scholar
  34. 34.
    Wiemken A., Schelleberg M., Urech R. 1979. Vacuoles: The sole compartments of digestive enzymes in yeast (Saccharomyces cerevisiae). Arch. Microbiol. 123, 23–25.CrossRefGoogle Scholar
  35. 35.
    Indge K.J. 1968. Polyphosphates of the yeast cell vacuole. J. Gen. Microbiol. 51, 447–455.PubMedGoogle Scholar
  36. 36.
    Westenberg B., Boller T., Wiemken A. 1989. Lack of arginine-and polyphosphate storage pools in a vacuole-deficient mutant (end 1) of S. cerevisiae. FEBS Lett. 254, 133–136.CrossRefGoogle Scholar
  37. 37.
    Shirahama K., Yazaki Y., Sakano K., Wada Y., Ohsumi Y. 1996. Vacuolar function in the phosphate homeostasis of the yeast Saccharomyces cerevisiae. Plant. Cell. Physiol. 37, 1090–1093.PubMedGoogle Scholar
  38. 38.
    Nunez C.G., Callieri A.S.1989. Studies on the polyphosphate cycle in Candida utilis. Effect of dilution rate and nitrogen source in continuous culture. Appl. Microbiol. Biotechnol. 31, 562–566.CrossRefGoogle Scholar
  39. 39.
    Lichko L.P., Okorokov L.A., Kulaev I.S. 1982. Participation of vacuoles in regulation of K+, Mg2+ and orthophosphate ions in cytoplasm of the yeast Saccharomyces carlsbergensis. Arch. Microbiol. 132, 289–293.CrossRefGoogle Scholar
  40. 40.
    Greenfeld N.J., Hussain M., Lenard J. 1987. Effect of growth state and amines on cytoplasm and vacuolar pH, phosphate and polyphosphate levels in Saccharomyces cerevisiae:A 31P-nuclear magnetic resonance study. Biochim. Biophys. Acta. 926, 205–214.PubMedGoogle Scholar
  41. 41.
    Castro C.D., Meehan A.J., Koretsky A.P., Domach M.M. 1995. In situ 31P nuclear magnetic resonance for observation of polyphosphate and catabolite responses of chemostat-cultivated Saccharomyces cerevisiae after alkalinization. Appl. Environ. Microbiol. 61, 4448–4453.PubMedGoogle Scholar
  42. 42.
    Lusby E.W., McLaughlin C.S. 1980. The metabolic properties of acid soluble polyphosphates in Saccharomyces cerevisiae. Mol. Gen. Genet. 178, 69–76.CrossRefPubMedGoogle Scholar
  43. 43.
    Beauvoit B., Rigonlet M., Guerin B., Canioni P. 1989. Polyphosphates as a source of high energy phosphates in yeast mitochondria: A P-NMR study. FEBS Lett. 252, 17–22.CrossRefGoogle Scholar
  44. 44.
    Pestov N.A., Kulakovskaya T.V., Kulaev I.S. 2004. Inorganic polyphosphate in mitochondria of Saccharomyces cerevisiae at phosphate limitation and phosphate excess. FEMS Yeast Res. 4, 643–648.CrossRefPubMedGoogle Scholar
  45. 45.
    Pestov N.A., Kulakovskaya T.V., Kulaev I.S. 2005. Effects of the PPN1 gene inactivation on exopolyphosphatases, inorganic polyphosphates and function of mitochondria in the yeast Saccharomyces cerevisiae. FEMS Yeast Res. (in press).Google Scholar
  46. 46.
    Kornberg A., Kornberg S., Simms E. 1956. Methaphosphate synthesis by enzyme from Escherichia coli. Biochim. Biophys. Acta. 20, 215–227.CrossRefPubMedGoogle Scholar
  47. 47.
    Zhang H., Ishige K., Kornberg A. 2002. A polyphosphate kinase (PPK2) widely conserved in bacteria. Proc. Natl. Acad. Sci. USA. 99, 16678–16683.CrossRefPubMedGoogle Scholar
  48. 48.
    Felter S., Stahl A.J.C. 1973. Enzymes du metabolisme des polyphosphates dans la levure: 3. Purification et proprietes de la polyphosphate-ADP-phosphotransferase. Biochimie. 55, 245–251.PubMedGoogle Scholar
  49. 49.
    Booth J.W., Guidotti G. 1995. An alleged yeast polyphosphate kinase is actually diadenosine-5′, 5‴-P1,P4-tetraphosphate α,β-phosphorylase. J. Biol. Chem. 270, 19377–19382.CrossRefPubMedGoogle Scholar
  50. 50.
    Shabalin Yu.A., Vagabov V.M., Tsiomenko A.B., Zemlyanukhina O.A., Kulaev I.S. 1977. Studies on polyphosphate kinase activity in yeast vacuoles. Biokhimiya. 42, 1642–1648.Google Scholar
  51. 51.
    Sethuraman A., Rao N.N., Kornberg A. 2001. The endopolyphosphatase gene: Essential in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 98, 8542–8547.CrossRefPubMedGoogle Scholar
  52. 52.
    Akiyama M., Crooke E., Kornberg A. 1993. An exopolyphosphatase of Escherichia coli. The enzyme and its ppx gene in a polyphosphate operon. J. Biol. Chem. 268, 633–639.PubMedGoogle Scholar
  53. 53.
    Keasling J.D., Bertsh L., Kornberg A. 1993. Guanosine pentaphosphate phosphohydrolase of Escherichia coli is a long-chain exopolyphosphatase. Proc. Natl. Acad. Sci. USA. 90, 7029–7033.PubMedGoogle Scholar
  54. 54.
    Reizer J., Reizer A., Saier M.H., Jr., Bork B., Sander C. 1993. Exopolyphosphate phosphatase and guanosine pentaphosphate phosphatase belong to the sugar kinase/actin/hsp 70 superfamily. Trends Biochem. Sci. 18, 247–248.CrossRefPubMedGoogle Scholar
  55. 55.
    Wurst H., Shiba T., Kornberg A. 1995. The gene for a major exopolyphosphatase of Saccharomyces cerevisiae. J. Bacteriol. 177, 898–906.PubMedGoogle Scholar
  56. 56.
    Andreeva N.A., Okorokov L.A. 1990. Some properties of highly purified cell wall polyphosphatase of the yeast Saccharomyces cerevisiae. Biokhimiya. 55, 2286–2292.Google Scholar
  57. 57.
    Wurst H., Kornberg A. 1994.A soluble exopolyphosphatase of Saccharomyces cerevisiae. J. Biol. Chem. 269, 10996–11001.PubMedGoogle Scholar
  58. 58.
    Andreeva N.A., Kulakovskaya T.V., Karpov A.V., Sidorov I.A., Kulaev I.S. 1998. Purification and properties of polyphosphatase from Saccharomyces cerevisiae cytosol. Yeast. 14, 383–390.CrossRefPubMedGoogle Scholar
  59. 59.
    Lichko L.P., Andreeva N.A., Kulakovskaya T.A., Kulaev I.S. 2003. Exopolyphosphatases of the yeast Saccharomyces cerevisiae. FEMS Yeast Res. 3, 233–238.CrossRefPubMedGoogle Scholar
  60. 60.
    Guranowski A., Starzynska E., Barnes L.D., Robinson A.K., Liu S. 1998. Adenosine 5′-tetraphosphate phosphohydrolase activity is an inherent property of soluble exopolyphosphatase from Saccharomyces cerevisiae. Biochim. Biophys. Acta. 1380, 232–238.PubMedGoogle Scholar
  61. 61.
    Andreeva N.A., Kulakovskaya T.V., Kulaev I.S. 2004. Purification and properties of exopolyphosphatase not encoded by the PPX1 gene from the Saccharomyces cerevisiae cytosol. Biokhimiya. 69, 480–487.Google Scholar
  62. 62.
    Lichko L.P., Kulakovskaya T.V., Kulaev I.S. 2004. Partial purification and characterization of exopolyphosphatase from the nuclei of a Saccharomyces cerevisiae strain with inactivated PPX1 gene encoding basic yeast polyphosphatase. Biokhimiya. 69, 338–343.Google Scholar
  63. 63.
    Belozersky A.N. 1959. Contribution to discussion at the symposium “The Origin of Life on Earth.” Moscow: Akad. Nauk SSSR, 370.Google Scholar
  64. 64.
    Phillips N.F.B., Horn P.J., Wood H.G. 1993. The polyphosphate and ATP-dependent glucokinase from Propionibacterium shermanii: Both activities are catalyzed by the same protein. Arch. Biochem. Biophys. 300, 309–319.CrossRefPubMedGoogle Scholar
  65. 65.
    Kawai S., Mori S., Mukai T., Suzuki S., Yamada T., Hashimoto W., Murata K. 2000. Inorganic polyphosphate/ATP-NAD kinase of Micrococcus flavus and Mycobacterium tuberculosis H37Rv. Biochem. Biophys. Res. Commun. 276, 57–63.CrossRefPubMedGoogle Scholar
  66. 66.
    Kawai S., Mori S., Mukai T., Hashimoto W., Murata K. 2001. Molecular characterization of Escherichia coli NAD kinase. Eur. J. Biochem. 268, 4359–4365.CrossRefPubMedGoogle Scholar
  67. 67.
    Bobyk M.A., Kulaev I.S. 1971. 1,3-Diphosphoglycerate: polyphosphate phosphotransferase: A new enzyme of Neurospora crassa. Biokhimiya. 36, 426–429.Google Scholar
  68. 68.
    Schuddemat J. de Boo R., van Leeuwen C.C.M., van den Broek P.J.A., van Steveninck J. 1989. Polyphosphate synthesis in yeast. Biochim. Biophys. Acta. 100, 191–198.Google Scholar
  69. 69.
    Vagabov V.M., Trilisenko L.V., Shchipanova I.N., Sibeldina L.A., Kulaev I.S. Changes in the length of inorganic polyphosphate chains depending on the growth stage of Saccharomyces cerevisiae. Mikrobiologiya. 67,188–193.Google Scholar
  70. 70.
    Vagabov V.M., Trilisenko L.V., Kulaev I.S. Dependence of inorganic polyphosphate chain length in yeast on orthophosphate content in the medium. Biokhimiya. 65, 414–420.Google Scholar
  71. 71.
    Kulakovskaya T.V., Andreeva N.A., Trilisenko L.V., Vagabov V.M., Kulaev I.S. 2004. Two exopolyphosphatases in Saccharomyces cerevisiae cytosol at different culture conditions. Process Biochem. 39, 1625–1630.CrossRefGoogle Scholar
  72. 72.
    Den Hollander J.A., Ugurbil T., Brown T.R., Shulman R.G. 1981. Phosphorus-31 nuclear magnetic resonance studies on the effect of oxygen upon glycolysis in yeast. Biochemistry. 20, 5871–5880.CrossRefPubMedGoogle Scholar
  73. 73.
    McGrath, J.W., Quinn J.P. 2000. Intracellular accumulation of polyphosphate by the yeast Candida humicola G-1 in response to acid pH. Appl. Environ. Microbiol. 66, 4068–4073.CrossRefPubMedGoogle Scholar
  74. 74.
    Loureiro-Dias M.C., Santos H. 1990. Effects of ethanol on Saccharomyces cerevisiae as monitored by in vivo 31P and 13C nuclear magnetic resonance. Arch. Microbiol. 153, 384–391.CrossRefPubMedGoogle Scholar
  75. 75.
    Herve M., Wietzerbin J., Lebourguais O., Tran-Dinh S. 1992. Effects of 2-deoxy-D-glucose on the glucose metabolism in Saccharomyces cerevisiae studied by multinuclear-NMR spectroscopy and biochemical methods. Biochimie. 74, 1103–1115.CrossRefPubMedGoogle Scholar
  76. 76.
    Reidl H.H., Grover T.A., Takemoto J.Y. 1989. 31P-NRM evidence for cytoplasmic acidification and phosphate extrusion in syringomycin-treated cells of Rhodotorula pilimana. Biochim. Biophys. Acta. 1010, 325–329.CrossRefPubMedGoogle Scholar
  77. 77.
    Lohmeier-Vogel E., Skoog K., Vogel H., Hahn-Hagerdal B. 1989. 31P Nuclear magnetic resonance study of the effect of azide on xylose fermentation by Candida tropicalis. Appl. Envinron. Microbiol. 55, 1974–1980.Google Scholar
  78. 78.
    Beauvoit B., Rigoulet M., Raffard G., Canioni P., Guerin B. 1991. Differential sensitivity of the cellular compartments of Saccharomyces cerevisiae to protonophoric uncoupler under fermentative and respiratory energy supply. Biochemistry. 30, 11212–11220.CrossRefPubMedGoogle Scholar
  79. 79.
    Trilisenko L.V., Andreeva N.A., Kulakovskaya T.V., Vagabov V.M., Kulaev I.S. 2003. Inhibitor analysis of polyphosphate metabolism in the yeast Saccharomyces cerevisiae under hypercompensation conditions. Biokhimiya. 68, 706–711.Google Scholar
  80. 80.
    Okorokov L.A., Andreeva N.A., Lichko L.P., Valiakhmetov A.Ya. 1983. Transmembrane gradient of K+ ions as an energy source in the yeast Saccharomyces carlsbergensis. Biochem. Int. 6, 463–472.PubMedGoogle Scholar
  81. 81.
    Lichko L., Kulakovskaya T., Kulaev I. 2004. Inactivation of endopolyphosphatase gene PPN1 results in inhibition of expression of exopolyphosphatase PPX1 and high-molecular-mass exopolyphosphatase not encoded by PPX1 in Saccharomyces cerevisiae. Biochim. Biophys. Acta. 1674, 98–102.PubMedGoogle Scholar
  82. 82.
    Ogawa N., DeRisi J., Brown P.O. 2000. New components of a system for phosphate accumulation and polyphosphate metabolism in Saccharomyces cerevisiae revealed by genomic expression analysis. Mol. Biol. Cell. 11, 4309–4321.PubMedGoogle Scholar
  83. 83.
    Persson B.L., Lagerstedt J.O., Pratt J.R., Pattison-Granberg J., Lundh K., Shokrollahzadeh S., Lundh F. 2003. Regulation of phosphate acquisition in Saccharomyces cerevisiae. Curr. Genet. 43, 225–244.CrossRefPubMedGoogle Scholar
  84. 84.
    Nishimura K., Yasumura K., Igarashi K., Kakinuma Y. 1999. Involvement of Spt7p in vacuolar polyphosphate level of Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 257, 835–838.CrossRefPubMedGoogle Scholar
  85. 85.
    Solimene R., Guerrini A.M., Donini P. 1980. Levels of acid-soluble polyphosphate in growing cultures of Saccharomyces cerevisiae. J. Bacteriol. 143, 6710–6714.Google Scholar
  86. 86.
    Karpichev I.V., Cornivelli L., Small G.M. 2002. Multiple regulatory roles of a novel Saccharomyces cerevisiae protein, encoded by YOUL002c, in lipid and phosphate metabolism. J. Biol. Chem. 277, 19609–19617.CrossRefPubMedGoogle Scholar
  87. 87.
    Kisselev L.L., Justesen J., Wolfson A.D., Frolova L.Y. 1998. Diadenosine oligophosphates (ApNA), a novel class of signalling molecules. FEBS Lett. 2427, 157–163.CrossRefGoogle Scholar

Copyright information

© MAIK “Nauka/Interperiodica” 2005

Authors and Affiliations

  • I. S. Kulaev
    • 1
    • 2
  • V. M. Vagabov
    • 2
  • T. V. Kulakovskaya
    • 2
  • N. A. Andreeva
    • 2
  • L. P. Lichko
    • 2
  • L. V. Trilisenko
    • 2
  1. 1.Biological FacultyMoscow State UniversityMoscowRussia
  2. 2.Skryabin Institute of Biochemistry and Physiology of MicroorganismsRussian Academy of SciencesPushchino, Moscow RegionRussia

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