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Accumulation of inorganic polyphosphates in Saccharomyces cerevisiae under nitrogen deprivation: Stimulation by magnesium ions and peculiarities of localization

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Abstract

The yeast Saccharomyces cerevisiae was shown to have a high potential as a phosphate-accumulating organism under growth suppression by nitrogen limitation. The cells took up over 40% of phosphate from the medium containing 30 mM glucose and 5 mM potassium phosphate and over 80% of phosphate on addition of 5 mM magnesium sulfate. The major part of accumulated Pi was reserved as polyphosphates. The content of polyphosphates was ∼57 and ∼75% of the phosphate accumulated by the cells in the absence and presence of magnesium ions, respectively. The content of long-chain polyphosphates increased in the presence of magnesium ions, 5-fold for polymers with the average length of ∼45 phosphate residues, 3.7-fold for polymers with the average chain length of ∼75 residues, and more than 10-fold for polymers with the average chain length of ∼200 residues. On the contrary, the content of polyphosphates with the average chain length of ∼15 phosphate residues decreased threefold. According to the data of electron and confocal microscopy and X-ray microanalysis, the accumulated polyphosphates were localized in the cytoplasm and vacuoles. The cytoplasm of the cells accumulating polyphosphates in the presence of magnesium ions had numerous small phosphorus-containing inclusions; some of them were associated with large electron-transparent inclusions and the cytoplasmic membrane.

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References

  1. Kulaev, I.S., Vagabov, V.M., and Kulakovskaya, T.V., Vysokomolekulyarnye neorganicheskie polifosfaty: biokhimiya, kletochnaya biologiya, biotekhnologiya (High-Molecular-Mass Inorganic Polyphosphates: Biochemistry and Cell Biology), Moscow: Nauchnyi Mir, 2005.

    Google Scholar 

  2. Docampo, R. and Moreno, S.N., The Acidocalcisome, Mol. Biochem. Parasitol., 2001, vol. 114, pp. 151–159.

    Article  PubMed  CAS  Google Scholar 

  3. Omelon, S.J. and Grynpas, M.D., Relationships between Polyphosphate Chemistry, Biochemistry and Apatite Biomineralization, Chem. Rev., 2008, vol. 208, pp. 4694–4715.

    Article  Google Scholar 

  4. Rao, N.N., Gomez-Garcia, M.R., and Kornberg, A., Inorganic Polyphosphate: Essential for Growth and Survival, Annu. Rev. Biochem., 2009, vol. 78, pp. 605–647.

    Article  PubMed  CAS  Google Scholar 

  5. Mino, T., Van Loosdrecht, M.C.M., and Heijnen, J.J., Microbiology and Biochemistry of the Enhanced Biological Phosphate Removal Process, Water Res., 1998, vol. 32, pp. 3193–3207.

    Article  CAS  Google Scholar 

  6. Keasling, J.D., Van Dien, S.J., Trelstad, P., Renninger, N., and McMahon, K., Application of Polyphosphate Metabolism to Environmental and Biotechnological Problems, Biokhimiya, 2000, vol. 65, no. 3, pp. 385–394 [Biochemistry (Moscow) (Engl. Transl.), vol. 65, no. 3, pp. 324–331].

    Google Scholar 

  7. Seviour, R.J., Mino, T., and Onuki, M., The Microbiology of Biological Phosphorus Removal in Activated Sludge, FEMS. Microbiol. Rev., 2003, vol. 27, pp. 99–127.

    Article  PubMed  CAS  Google Scholar 

  8. Lopez-Vazques, C.M., Hooijmans, C.M., Brdjanivic, D., Gijzen, H.J., and van Loosdrecht, M.C., A Practical Method for Quantification of PAO and GAO Populations in Activated Sludge Systems, Water Environ. Res., 2007, vol. 79, pp. 2487–2498.

    Article  Google Scholar 

  9. Melasniemi, H. and Hernesmaa, A., Yeast Spores Seem to Be Involved in Biological Phosphate Removal: a Microscopic in situ Case Study, Microbiology (UK), 2000, vol. 146, pp. 701–707.

    CAS  Google Scholar 

  10. McGrath, J.W. and Quinn, J.P., Intracellular Accumulation of Polyphosphate by the Yeast Candida humicola G-1 in Response to Acid pH, Appl. Environ. Microbiol., 2000, vol. 66, pp. 4068–4073.

    Article  PubMed  CAS  Google Scholar 

  11. McGrath, J.W., Kulakova, A.N., Kulakov, L.A., and Quinn, J.P., In vitro Detection and Characterisation of a Polyphosphate Synthesising Activity in the Yeast Candida humicola G-1, Res. Microbiol., 2005, vol. 156, pp. 485–491.

    Article  PubMed  CAS  Google Scholar 

  12. Watanabe, T., Ozaki, N., Iwashita, K., Fujii, T., and Iefuji, H., Breeding of Wastewater Treatment Yeasts That Accumulate High Concentration of Phosphorus, Appl. Microbiol. Biotechnol., 2008, vol. 80, pp. 331–338.

    Article  PubMed  CAS  Google Scholar 

  13. Kulakovskaya, T.V., Andreeva, N.A., Karpov, A.V., Sidorov, I.A., and Kulaev, I.S., Hydrolysis of Tripolyphosphate by Purified Exopolyphosphatase from Saccharomyces cerevisiae Cytosol: Kinetic Model, Biokhimiya, 1999, vol. 64, no. 9, pp. 1180–1184 Biochemistry (Moscow) (Engl. Transl.), vol. 64, no. 9, pp. 990–993].

    Google Scholar 

  14. Vagabov, V.M., Trilisenko, L.V., and Kulaev, I.S., Dependence of Inorganic Polyphosphate Chain Length on the Orthophosphate Content in the Culture Medium of the Yeast Saccharomyces cerevisiae, Biokhimiya, 2000, vol. 65, pp. 414–420 Biochemistry (Moscow) (Engl. Transl.), vol. 65, no. 3, pp. 349–354].

    Google Scholar 

  15. Lichko, L., Kulakovskaya, T., Pestov, N., and Kulaev, I., Inorganic Polyphosphates and Exopolyphosphatases in Cell Compartments of the Yeast Saccharomyces cerevisiae under Inactivation of PPX1 and PPN1 Genes, Biosci. Rep., 2006, vol. 26, pp. 45–54.

    Article  PubMed  CAS  Google Scholar 

  16. Reynolds, E.S., The Use of Lead Citrate at High pH as an Electron Opaque Stain in Electron Microscopy, J. Cell Biol., 1963, vol. 17, pp. 208–213.

    Article  PubMed  CAS  Google Scholar 

  17. Ryazanova, L.P., Smirnov, A.V., Kulakovskaya, T.V., and Kulaev, I.S., Decrease of Phosphate Concentration in the Medium by Brevibacterium casei Cells, Mikrobiologiya, 2007, vol. 76, no. 6, pp. 752–758 [Microbiology (Engl. Transl.), vol. 76, no. 6, pp. 663–668].

    Google Scholar 

  18. Ryazanova, L.P., Suzina, N.E., Kulakovskaya, T.V., and Kulaev, I.S., Phosphate Accumulation of Acetobacter ylinum, Arch. Microbiol., 2009, vol. 191, pp. 467–471.

    Article  PubMed  CAS  Google Scholar 

  19. Smirnov, A., Suzina, N., Chudinova, N., Kulakovskaya, T., and Kulaev, I., Formation of Insoluble Magnesium Phosphates during Growth of the Archaea Halorubrum distributum and Halobacterium salinarium and the Bacterium Brevibacterium antiquum, FEMS Microbiol. Ecol., 2005, vol. 52, pp. 129–137.

    Article  PubMed  CAS  Google Scholar 

  20. Van Veen, H.W., Abee, T., Kortstee, G.J.J., Konings, W.N., and Zehnder, A.J.B., Characterization of Two Phosphate Transport Systems in Acinetobacter johnsonii Strain 210A, J. Bacteriol., 1993, vol. 175, pp. 200–206.

    PubMed  Google Scholar 

  21. Vagabov, V.M., Trilisenko, L.V., Kulakovskaya, T.V., and Kulaev, I.S., Effect of Carbon Source on Polyphosphate Accumulation in Saccharomyces cerevisiae, FEMS Yeast Res., 2008, vol. 8, pp. 877–882.

    Article  PubMed  CAS  Google Scholar 

  22. Vorisek, J., Knotkova, A., and Kotyk, A., Fine Cytochemical Localization of Polyphosphates in the Yeast Saccharomyces cerevisiae, Zentralbl. Mikrobiol., 1982, vol. 137, pp. 421–432.

    PubMed  CAS  Google Scholar 

  23. Hothorn, M., Neumann, H., Lenherr, E.D., Wehner, M., Rybin, V., Hassa, P.O., Uttrnweiler, A., Reinhardt, M., Schmidt, A., Seiler, J., Ladurner, A.G., Hermann, C., Scheffzek, K., and Mayer, A., Catalytic Core of a Membrane-Associated Eukaryotic Polyphosphate Polymerase, Science, 2009, vol. 324, pp. 513–516.

    Article  PubMed  CAS  Google Scholar 

  24. Serafim, L.S., Lemos, O.C., Levantesi, C., Tandoi, V., Santos, H., and Reis, M.A., Methods for Detection and Visualization of Intracellular Polymers Stored by Polyphosphate-Accumulating Microorganisms, J. Microbiol. Methods, 2002, vol. 51, pp. 1–18.

    Article  PubMed  CAS  Google Scholar 

  25. Abramov, A.Y., Fraley, C., Diao, C.T., Winkfein, R., Colinos, M.A., Duchen, M.R., French, R.J., and Pavlov, E., Targeted Polyphosphatase Expression Alters Mitochondrial Metabolism and Inhibits Calcium-Dependent Cell Death, Proc. Natl. Acad. Sci. U.S.A., 2007, vol. 104, pp. 18091–18096.

    Article  PubMed  CAS  Google Scholar 

  26. Puchkov, E.O., Brownian Motion of Polyphosphate Complexes in Yeast Vacuoles: Characterization by Fluorescence Microscopy with Image Analysis, Yeast, 2010, vol. 27, pp. 309–315.

    PubMed  CAS  Google Scholar 

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Correspondence to N. V. Kulakovskaya.

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Original Russian Text © N.A. Breus, L.P. Ryazanova, N.E. Suzina, N.V. Kulakovskaya, A.Ya. Valiakhmetov, V.A. Yashin, V.V. Sorokin, I.S. Kulaev, 2011, published in Mikrobiologiya, 2011, Vol. 80, No. 5, pp. 612–618.

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Breus, N.A., Ryazanova, L.P., Suzina, N.E. et al. Accumulation of inorganic polyphosphates in Saccharomyces cerevisiae under nitrogen deprivation: Stimulation by magnesium ions and peculiarities of localization. Microbiology 80, 624–630 (2011). https://doi.org/10.1134/S002626171105002X

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