Skip to main content
Log in

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

  • Review and Experimantal Articles
  • Published:
Molecular Biology Aims and scope Submit manuscript

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.

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.

Similar content being viewed by others

REFERENCES

  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. Bukhovich E, Belozersky A.N. 1958. Some aspects of polyphosphate formation in yeast cells. Biokhimiya. 23, 254–259.

    Google Scholar 

  3. Kulaev I.S., Belozersky A.N. 1962. Condensed inorganic phosphates in metabolism: 1. Izv. Akad. Nauk SSSR. 3, 354–368.

    Google Scholar 

  4. Liss E., Langen P. 1962. Versuche zur Polyphosphat-Uberkompensation in Heffenzellen nach Phosphatverarmung. Arch. Microbiol. 41, 383–392.

    Google Scholar 

  5. Harold F.M. 1966. Inorganic polyphosphates in biology: structure, metabolism, and functions. Bacteriol. Rev. 30, 772–794.

    PubMed  Google Scholar 

  6. Kulaev I.S. 1975. Biokhimiya neorganicheskikh polifosfatov (Biochemistry of Inorganic Polyphosphates). Moscow: Izd. Mosk. Gos. Univ.

    Google Scholar 

  7. Kulaev I.S. 1979. The Biochemistry of Inorganic Polyphosphates. Wiley.

  8. Kulaev I.S., Vagabov V.M. 1983. Polyphosphate metabolism in microorganisms. Adv. Microbiol. Physiol. 24, 83–171.

    Google Scholar 

  9. Wood H.G., Clark J.E. 1988. Biological aspects of inorganic polyphosphates. Ann. Rev. Biochem. 57, 235–260.

    Article  PubMed  Google Scholar 

  10. Kornberg A. 1995. Inorganic polyphosphate: Toward making a forgotten polymer unforgettable. J. Bacteriol. 177, 491–496.

    PubMed  Google Scholar 

  11. Kornberg A., Rao N.N., Ault-Riche D. 1999. Inorganic Polyphosphate: a molecule with many functions. Ann. Rev. Biochem. 68, 89–125.

    Article  PubMed  Google Scholar 

  12. Kulaev I., Vagabov V., Kulakovskaya T. 1999. New aspects of polyphosphate metabolism and function. J. Biosci. Bioeng. 88, 111–129.

    Article  Google Scholar 

  13. Kulaev I.S., Kulakovskaya T.V. 2000. Polyphosphate and phosphate pump. Ann. Rev. Microbiol. 54, 709–735.

    Article  Google Scholar 

  14. Kulaev I., Vagabov V., Kulakovskaya T. 2004. The Biochemistry of Inorganic Polyphosphates, 2nd ed. Wiley.

  15. Belozersky A.N. 1945. On the chemical nature of volutin. Mikrobiologiya. 14, 29–33.

    Google Scholar 

  16. Wiame J.M. 1947. Etude d’une substance polyphosphoree, basophillie et metachromatique chez les levures. Biochim. Biophys. Acta. 1. 234–255.

    Article  Google Scholar 

  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. 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.

    PubMed  Google Scholar 

  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. 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.

    PubMed  Google Scholar 

  21. Rosh R. 2000. Transmembrane ion transport by polyphosphate-poly-(β)-hydroxybutyrate complexes. Biokhimiya. 65, 335–353.

    Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

  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.

    PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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. Vagabov V.M. 1988. Biosintez uglevodnykh komponentov kletochnoi stenki u drozzhei (Biosynthesis of Cell Wall Carbohydrates in Yeast). Pushchino: ONTI NTsBI.

    Google Scholar 

  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. 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. 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. Shabalin Yu.A., Kulaev I.S. 1989. Solubilization and properties of yeast dolichyldiphosphate: polyphosphate phosphotrasnferase. Biokhimiya. 54, 68–75.

    Google Scholar 

  33. Matile P.1978. Biochemistry and function of vacuoles. Ann. Rev. Plant Physiol. 29, 193–213.

    Google Scholar 

  34. Wiemken A., Schelleberg M., Urech R. 1979. Vacuoles: The sole compartments of digestive enzymes in yeast (Saccharomyces cerevisiae). Arch. Microbiol. 123, 23–25.

    Article  Google Scholar 

  35. Indge K.J. 1968. Polyphosphates of the yeast cell vacuole. J. Gen. Microbiol. 51, 447–455.

    PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  42. Lusby E.W., McLaughlin C.S. 1980. The metabolic properties of acid soluble polyphosphates in Saccharomyces cerevisiae. Mol. Gen. Genet. 178, 69–76.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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).

  46. Kornberg A., Kornberg S., Simms E. 1956. Methaphosphate synthesis by enzyme from Escherichia coli. Biochim. Biophys. Acta. 20, 215–227.

    Article  PubMed  Google Scholar 

  47. Zhang H., Ishige K., Kornberg A. 2002. A polyphosphate kinase (PPK2) widely conserved in bacteria. Proc. Natl. Acad. Sci. USA. 99, 16678–16683.

    Article  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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. Sethuraman A., Rao N.N., Kornberg A. 2001. The endopolyphosphatase gene: Essential in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 98, 8542–8547.

    Article  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  55. Wurst H., Shiba T., Kornberg A. 1995. The gene for a major exopolyphosphatase of Saccharomyces cerevisiae. J. Bacteriol. 177, 898–906.

    PubMed  Google Scholar 

  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. Wurst H., Kornberg A. 1994.A soluble exopolyphosphatase of Saccharomyces cerevisiae. J. Biol. Chem. 269, 10996–11001.

    PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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. 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. Belozersky A.N. 1959. Contribution to discussion at the symposium “The Origin of Life on Earth.” Moscow: Akad. Nauk SSSR, 370.

    Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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. 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. 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.

  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.

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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. 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.

    Article  PubMed  Google Scholar 

  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. 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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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. 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.

    Article  PubMed  Google Scholar 

  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.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

__________

Translated from Molekulyarnaya Biologiya, Vol. 39, No. 4, 2005, pp. 567–580.

Original Russian Text Copyright © 2005 by Kulaev, Vagabov, Kulakovskaya, Andreeva, Lichko, Trilisenko.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kulaev, I.S., Vagabov, V.M., Kulakovskaya, T.V. et al. Specific Features of Metabolism and Functions of High-Molecular Inorganic Polyphosphates in Yeasts as Representatives of Lower Eukaryotes. Mol Biol 39, 482–494 (2005). https://doi.org/10.1007/s11008-005-0065-1

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11008-005-0065-1

Key words

Navigation