Advertisement

Biochemistry (Moscow)

, Volume 79, Issue 13, pp 1602–1614 | Cite as

Diversity of phosphorus reserves in microorganisms

  • T. V. KulakovskayaEmail author
  • L. P. Lichko
  • L. P. Ryazanova
Review

Abstract

Phosphorus compounds are indispensable components of the Earth’s biomass metabolized by all living organisms. Under excess of phosphorus compounds in the environment, microorganisms accumulate reserve phosphorus compounds that are used under phosphorus limitation. These compounds vary in their structure and also perform structural and regulatory functions in microbial cells. The most common phosphorus reserve in microorganism is inorganic polyphosphates, but in some archae and bacteria insoluble magnesium phosphate plays this role. Some yeasts produce phosphomannan as a phosphorus reserve. This review covers also other topics, i.e. accumulation of phosphorus reserves under nutrient limitation, phosphorus reserves in activated sludge, mycorrhiza, and the role of mineral phosphorus compounds in mammals.

Key words

microorganism phosphorus inorganic polyphosphate magnesium phosphate phosphomannan EBPR limited growth phosphorus reserve 

Abbreviations

Pi

orthophosphate

polyP

inorganic polyphosphates

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Miller, S. L., and Parris, M. (1964) Synthesis of pyrophosphate under primitive earth conditions, Nature, 204, 1248–1249.Google Scholar
  2. 2.
    Beck, A., and Orgel, L. E. (1965) The formation of condensed phosphate in aqueous solution, Proc. Natl. Acad. Sci. USA, 54, 664–669.PubMedCentralPubMedGoogle Scholar
  3. 3.
    Lohmann, R., and Orgel, L. E. (1968) Prebiotic synthesis: phosphorylation in aqueous solution, Science, 161, 64–66.Google Scholar
  4. 4.
    Osterberg, R., and Orgel, L. E. (1972) Polyphosphate and trimetaphosphate formation under potentially perbiotic conditions, J. Mol. Evol., 1, 241–252.PubMedGoogle Scholar
  5. 5.
    Kulaev, I. S. (1975) Biochemistry of Inorganic Polyphosphates [in Russian], MGU Publishers, Moscow.Google Scholar
  6. 6.
    Miller, S. L. (1986) Current status of the prebiotic synthesis of small molecules, Chem. Scripta, 26B, 5–11.Google Scholar
  7. 7.
    Oro, J., Miller, S. L., and Lazcano, A. (1990) The origin and early evolution of life on Earth, Ann. Rev. Earth Planet Sci., 18, 317–356.Google Scholar
  8. 8.
    Kornberg, A. (1995) Inorganic polyphosphate: toward making a forgotten polymer unforgettable, J. Bacteriol., 177, 491–496.PubMedCentralPubMedGoogle Scholar
  9. 9.
    Arrhenius, G., Sales, B., Mojzsis, S., and Lee, T. (1997) Entropy and charge in molecular evolution: the case of phosphate, J. Theor. Biol., 187, 503–522.PubMedGoogle Scholar
  10. 10.
    Baltscheffsky, H. (1997) Major “Anastrophes” in the origin and early evolution of biological energy conversion, J. Theor. Biol., 187, 495–501.PubMedGoogle Scholar
  11. 11.
    De Graaf, R. M., and Schwartz, A. W. (2000) Reduction and activation of phosphate on the primitive earth, Origin Life Evol. Biospheres, 30, 405–410.Google Scholar
  12. 12.
    Spirin, A. S. (2001) Protein biosynthesis, the world of RNA, and life origin, Vestnik RAN, 71, 146–153.Google Scholar
  13. 13.
    Kulaev, I. S., Vagabov, V. M., and Kulakovskaya, T. V. (2005) High Molecular Weight Inorganic Polyphosphates: Biochemistry, Cell Biology, Biotechnology [in Russian], Nauchnyi Mir, Moscow.Google Scholar
  14. 14.
    Galimov, E. M. (2006) Phenomenon of Life. Between Equilibrium and Nonlinearity. Origin and Principles of Evolution [in Russian], URSS Publisher, Moscow.Google Scholar
  15. 15.
    Cavalier-Smith, T. (2006) Cell evolution and Earth history: stasis and revolution, Philos. Trans. R. Soc. Lond. B. Biol. Sci., 361, 969–1006.PubMedCentralPubMedGoogle Scholar
  16. 16.
    Wolfe-Simon, F., Switzer Blum, J., Kulp, T. R., Gordon, G. W., Hoeft, S. E., Pett-Ridge, J., Stolz, J. F., Webb, S. M., Weber, P. K., Davies, P. C., Anbar, A. D., and Oremland, R. S. (2011) A bacterium that can grow by using arsenic instead of phosphorus, Science, 332, 1163–1166.PubMedGoogle Scholar
  17. 17.
    Erb, T. J., Kiefer, P., Hattendorf, B., Gunther, D., and Vorholt, J. A. (2012) GFAJ-1 is an arsenate-resistant, phosphate-dependent organism, Science, 337, 467–470.PubMedGoogle Scholar
  18. 18.
    Rao, N. N., and Torriani, A. (1990) Molecular aspects of phosphate transport in Escherichia coli, Mol. Microbiol., 4, 1083–1090.PubMedGoogle Scholar
  19. 19.
    Van Veen, H. W., Abee, T., Kortstee, G. J. J., Konings, W. N., and Zehnder, A. J. B. (1994) Translocation of metal phosphate via the phosphate inorganic transport system of Escherichia coli, Biochemistry, 33, 1766–1770.PubMedGoogle Scholar
  20. 20.
    Harris, R. M., Webb, D. C., Howitt, S. M., and Cox, G. B. (2001) Characterization of PitA and PitB from Escherichia coli, J. Bacteriol., 183, 5008–5014.PubMedCentralPubMedGoogle Scholar
  21. 21.
    Spira, B., Aguena, M., de Castro Oliveira, J. V., and Yagil, E. (2010) Alternative promoters in the pst operon of Escherichia coli, Mol. Genet. Genom., 284, 489–498.Google Scholar
  22. 22.
    Persson, B. L., Lagerstedt, J. O., Pratt, J. R., Pattison-Granberg, J., Lundh, K., Shokrollahzadeh, S., and Lundh, F. (2003) Regulation of phosphate acquisition in Saccharomyces cerevisiae, Curr. Genet., 43, 225–244.PubMedGoogle Scholar
  23. 23.
    Dick, C. F., Dos-Santos, A. L., and Meyer-Fernandes, J. R. (2014) Inorganic phosphate uptake in unicellular eukaryotes, Biochim. Biophys. Acta, 1840, 2123–2127.PubMedGoogle Scholar
  24. 24.
    Smirnov, A. V., Suzina, N. E., Kulakovskaya, T. V., and Kulaev, I. S. (2002) Magnesium orthophosphate — the novel form of phosphate reservation in the halophilic archaeon Halobacterium salinarium, Mikrobiologiya, 71, 786–793.Google Scholar
  25. 25.
    Smirnov, A. V. (2003) Phosphate Uptake and Reservation by Some Archaea and Bacteria: Candidate’s dissertation [in Russian], Pushchino.Google Scholar
  26. 26.
    Smirnov, A., Suzina, N., Chudinova, N., Kulakovskaya, T., and Kulaev, I. (2005) Formation of insoluble phosphate during growth of the archae Halorubrum distributum and Halobacterium salinarium and the bacterium Brevibacterium antiquum, FEMS Microbiol. Ecol., 52, 129–137.PubMedGoogle Scholar
  27. 27.
    Ryazanova, L. P., Suzina, N. E., Kulakovskaya, T. V., and Kulaev, I. S. (2009) Phosphate accumulation of Acetobacter xylinum, Arch. Microbiol., 191, 467–471.PubMedGoogle Scholar
  28. 28.
    Gerasimenko, L. M., Goncharova, I. V., and Zaytseva, L. V. (1998) The influence of phosphorus content in the medium on cyanobacterial growth and mineralization, Mikrobiologiya, 67, 249–254.Google Scholar
  29. 29.
    Goncharova, I. V., and Gerasimenko, L. M. (1993) The dynamics of inorganic phosphorus uptake by the cells of Microcoleus chthonoplastes, Mikrobiologiya, 62, 1048–1055.Google Scholar
  30. 30.
    Kornberg, A., Rao, N. N., and Ault-Riche, D. (1999) Inorganic polyphosphate: a molecule with many functions, Ann. Rev. Biochem., 68, 89–125.PubMedGoogle Scholar
  31. 31.
    Reusch, R. N. (2000) Transmembrane ion transport by polyphosphate/poly-(R)-3-hydroxybutyrate complexes, Biochemistry (Moscow), 65, 280–295.Google Scholar
  32. 32.
    Rao, N. N., Gomez-Garcia, M. R., and Kornberg, A. (2009) Inorganic polyphosphate: essential for growth and survival, Ann. Rev. Biochem., 78, 605–647.PubMedGoogle Scholar
  33. 33.
    Harold, F. M. (1966) Inorganic polyphosphates in biology: structure, metabolism, and functions, Bacteriol. Rev., 30, 772–794.PubMedCentralPubMedGoogle Scholar
  34. 34.
    Kulaev, I. S., and Vagabov, V. M. (1983) Polyphosphate metabolism in microorganisms, Adv. Microbiol. Physiol., 24, 83–171.Google Scholar
  35. 35.
    Wood, H. G., and Clark, J. E. (1988) Biological aspects of inorganic polyphosphates, Ann. Rev. Biochem., 57, 235–260.PubMedGoogle Scholar
  36. 36.
    Nesmeyanova, M. A. (2000) Polyphosphates and enzymes of polyphosphate metabolism in Escherichia coli, Biochemistry (Moscow), 65, 309–314.Google Scholar
  37. 37.
    Deinema, M. H., Habers, L. H. A., Scholten, J., Turkstra, E., and Webers, H. A. A. M. (1980) The accumulation of polyphosphate in Acinetobacter spp., FEMS Microbiol. Lett., 9, 275–279.Google Scholar
  38. 38.
    Lindner, S. N., Knebel, S., Pallerla, S. R., Schoberth, S. M., and Wendisch, V. F. (2010) Cg2091 encodes a polyphosphate/ATP-dependent glucokinase of Corynebacterium glutamicum, Appl. Microbiol. Biotechnol., 87, 703–713.PubMedGoogle Scholar
  39. 39.
    Szymona, M. (1957) Utilization of inorganic polyphosphates for phosphorylation of glucose in Micobacterium phlei, Bull. Acad. Pol. Sci. Ser. Sci. Biol., 5, 379–381.Google Scholar
  40. 40.
    Hsieh, P. C., Shenoy, B. C., Samols, D., and Phillips, N. F. B. (1996) Cloning, expression and characterization of polyphosphate glucokinase from Mycobacterium tuberculosis, J. Biol. Chem., 271, 4909–4915.PubMedGoogle Scholar
  41. 41.
    Kawai, S., Mori, S., Mukai, T., Suzuki, S., Yamada, T., Hashimoto, W., and Murata, K. (2000) Inorganic polyphosphate/ATP-NAD kinase of Micrococcus flavus and Mycobacterium tuberculosis H37Rv, Biochem. Biophys. Res. Commun., 276, 57–63.PubMedGoogle Scholar
  42. 42.
    Mori, S., Yamasaki, M., Maruyama, Y., Momma, K., Kawai, S., Hashimoto, W., Mikami, B., and Murata, K. (2004) Crystallographic studies of Mycobacterium tuberculosis polyphosphate/ATP-NAD kinase complexed with NAD, J. Biosci. Bioeng., 98, 391–393.PubMedGoogle Scholar
  43. 43.
    Mukai, T., Kawai, S., Matsukawa, H., Matuo, Y., and Murata, K. (2003) Characterization and molecular cloning of a novel enzyme, inorganic polyphosphate/ATP-glucomannokinase, of Arthrobacter sp. strain KM, Appl. Environ. Microbiol., 69, 3849–3857.PubMedCentralPubMedGoogle Scholar
  44. 44.
    Kortstee, G. J. J., Appeldoorn, K. J., Bonting, C. F. C., van Niel, E. W. J., and van Veen, H. W. (2000) Recent developments in the biochemistry and ecology of enhanced biological phosphorus removal, Biochemistry (Moscow), 65, 332–340.Google Scholar
  45. 45.
    Mino, T. (2000) Microbial selection of polyphosphate-accumulating bacteria in activated sludge wastewater treatment processes for enhanced biological phosphate removal, Biochemistry (Moscow), 65, 341–348.Google Scholar
  46. 46.
    Keasling, J. D., van Dien, S. J., Trelstad, P., Renninger, N., and McMahon, K. (2000) Application of polyphosphate metabolism to environmental and biotechnological problems, Biochemistry (Moscow), 65, 324–331.Google Scholar
  47. 47.
    Vagabov, V. M., Trilisenko, L. V., Shchipanova, I. N., Sibeldina, L. A., and Kulaev, I. S. (1998) Variation of inorganic polyphosphate chain length depending on Saccharomyces cerevisiae growth stage, Mikrobiologiya, 67, 193–198.Google Scholar
  48. 48.
    Lichko, L., Kulakovskaya, T., Pestov, N., and Kulaev, I. (2006) Inorganic polyphosphates and exopolyphosphatases in cell compartments of the yeast Saccharomyces cerevisiae under inactivation of PPX1 and PPN1 genes, Biosci. Rep., 26, 45–54.PubMedGoogle Scholar
  49. 49.
    Vagabov, V. M., Trilisenko, L. V., and Kulaev, I. S. (2000) Dependence of inorganic polyphosphate chain length on the orthophosphate content in the culture medium of the yeast Saccharomyces cerevisiae, Biochemistry (Moscow), 65, 349–354.Google Scholar
  50. 50.
    Kalebina, T. S., Egorov, S. N., Arbatsky, N. P., Bezsonov, E. E., Gorkovsky, A. A., and Kulaev, I. S. (2008) On the role of high molecular polyphosphates in the activation of glucan transferase Bgl2p from the cell wall of the yeast Saccharomyces cerevisiae, Dokl. Akad. Nauk, 420, 695–698.Google Scholar
  51. 51.
    Ivanov, A. Yu., Vagabov, V. M., Fomchenkov, V. M., and Kulaev, I. S. (1996) Investigation of the influence of cell wall polyphosphates on sensitivity of the yeast Saccharomyces carlsbergensis to the damage by cetyl trimethyl ammonium bromide, Mikrobiologiya, 65, 611–616.Google Scholar
  52. 52.
    McGrath, J. W., and 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.PubMedCentralPubMedGoogle Scholar
  53. 53.
    McGrath, J. W., Kulakova, A. N., Kulakov, L. A., and Quinn, J. P. (2005) In vitro detection and characterization of a polyphosphate synthesizing activity in the yeast Candida humicola G-1, Res. Microbiol., 156, 485–491.PubMedGoogle Scholar
  54. 54.
    Watanabe, T., Ozaki, N., Iwashita, K., Fujii, T., and Lefuji, H. (2008) Breeding of wastewater treatment yeasts that accumulate high concentration of phosphorus, Appl. Microbiol. Biotechnol., 80, 331–338.PubMedCentralPubMedGoogle Scholar
  55. 55.
    Potekhina, N. V., Streshinskaya, G. M., Tul’skaya, E. M., Kozlova, Yu. I., Senchenkova, S. N., and Shashkov, A. S. (2011) Phosphate-containing cell wall polymers of bacilli, Biochemistry (Moscow), 76, 745–754.Google Scholar
  56. 56.
    Grant, W. D. (1979) Cell wall teichoic acid as a reserve phosphate source in Bacillus subtilis, J. Bacteriol., 137, 35–43.PubMedCentralPubMedGoogle Scholar
  57. 57.
    Bhavsar, A. P., Erdman, L. K., Schertzer, J. W., and Brown, E. D. (2004) Teichoic acid is an essential polymer in Bacillus subtilis that is functionally distinct from teichuronic acid, J. Bacteriol., 186, 7865–7873.PubMedCentralPubMedGoogle Scholar
  58. 58.
    Brown, S., Santa Maria, J. P., Jr., and Walker, S. (2013) Wall teichoic acids of gram-positive bacteria, Ann. Rev. Microbiol., 67, 313–336.Google Scholar
  59. 59.
    Slodki, M. E. (1963) Structure of Hansenula capsulata NRRL Y-1842 phosphomannan, Biochim. Biophys. Acta, 69, 96–102.PubMedGoogle Scholar
  60. 60.
    Avigad, G., and Kalina, M. (1979) Effect of orthophosphate limitation on the production of phosphomannan by Hansenula capsulata, FEMS Microbiol. Lett., 6, 111–114.Google Scholar
  61. 61.
    Lichko, L. P., Kulakovskaya, T. V., and Kulaev, I. S. (2013) Extracellular phosphomannan as a phosphate reserve in the yeast Kuraishia capsulata, Biochemistry (Moscow), 78, 674–677.Google Scholar
  62. 62.
    Kuroda, A. (2006) A polyphosphate-Lon protease complex in the adaptation of Escherichia coli to amino acid starvation, Biosci. Biotechnol. Biochem., 70, 325–331.PubMedGoogle Scholar
  63. 63.
    Ryazanova, L. P., Smirnov, A. V., Kulakovskaya, T. V., and Kulaev, I. S. (2007) Reduction of phosphate concentration in the medium by the cells of Brevibacterium casei, Mikrobiologiya, 76, 752–758.Google Scholar
  64. 64.
    Breus, N. A., Ryazanova, L. P., Dmitriev, V. V., Kulakovskaya, T. V., and Kulaev, I. S. (2012) Accumulation of phosphate and polyphosphate by Cryptococcus humicola and Saccharomyces cerevisiae in the absence of nitrogen, FEMS Yeast Res., 12, 617–624.PubMedGoogle Scholar
  65. 65.
    Van Niel, E. W. J., De Best, J. H., Kets, E. P. W., Bonting, C. F. C., and Kortstee, G. J. J. (1999) Polyphosphate formation by Acinetobacter johnsonii 210A: effect of cellular energy status and phosphate-specific transport system, Appl. Microbiol. Biotechnol., 51, 639–646.Google Scholar
  66. 66.
    Santos, M. M., Lemos, P. C., Reis, M. A. M., and Santos, H. (1999) Glucose metabolism and kinetics of phosphorus removal by the fermentative bacterium Microlunatus phosphovorus, Appl. Environ. Microbiol., 65, 3920–3928.PubMedCentralPubMedGoogle Scholar
  67. 67.
    Zilles, J. L., Peccia, J., Kim, M. W., Hung, C. H., and Noguera, D. R. (2002) Involvement of Rhodocyclus-related organisms in phosphorus removal in full scale wastewater treatment plants, Appl. Environ. Microbiol., 68, 2763–2769.PubMedCentralPubMedGoogle Scholar
  68. 68.
    Breus, N. A., Ryazanova, L. P., Suzina, N. E., Kulakovskaya, T. V., Valiakhmetov, A. Ya., Yashin, V. A., Sorokin, V. V., and Kulaev, I. S. (2010) Accumulation of inorganic polyphosphates in Saccharomyces cerevisiae under nitrogen deficiency: stimulation by magnesium ions and peculiarities of localization, Mikrobiologiya, 80, 612–618.Google Scholar
  69. 69.
    Diaz, J., Ingall, E., Benitez-Nelson, C., Paterson, D., de Jonge, M. D., McNulty, I., and Brandes, J. A. (2008) Marine polyphosphate: a key player in geologic phosphorus sequestration, Science, 320, 652–655.PubMedGoogle Scholar
  70. 70.
    Omelon, S., Ariganello, M., Bonucci, E., Grynpas, M., and Nanci, A. (2013) A review of phosphate mineral nucleation in biology and geobiology, Calcif. Tissue Int., 93, 382–396.PubMedCentralPubMedGoogle Scholar
  71. 71.
    Karl, D. M. (2014) Microbially mediated transformations of phosphorus in the sea: new views of an old cycle, Ann. Rev. Marine Sci., 6, 279–337.Google Scholar
  72. 72.
    Schulz, H. N., and Schulz, H. D. (2005) Large sulfur bacteria and the formation of phosphorite, Science, 307, 416–418.PubMedGoogle Scholar
  73. 73.
    Goldhammer, T., Bruchert, V., Ferdelman, T. G., and Zabel, M. (2010) Microbial sequestration of phosphorus in anoxic upwelling sediments, Nat. Geosci., 3, 557–561.Google Scholar
  74. 74.
    Brock, J., and Schulz-Vogt, H. N. (2011) Sulfide induced phosphate release from polyphosphate in cultures of marine Beggitoa strain, ISME J., 5, 497–506.PubMedCentralPubMedGoogle Scholar
  75. 75.
    Dyhrman, S. T., Jenkins, B. D., Rynearson, T. A., Saito, M. A., Mercier, M. L., Alexander, H., Whitney, L. P., Drzewianowski, A., Bulygin, V. V., Bertrand, E. M., Wu, Z., Benitez-Nelson, C., and Heithoff, A. (2012) The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response, PLoS One, 7, e33768; DOI: 0.1371/journal.pone.0033768.PubMedCentralPubMedGoogle Scholar
  76. 76.
    Temperton, B., Gilbertm, J. A., Quinn, J. P., and McGrath, J. W. (2011) Novel analysis of oceanic surface water metagenomes suggests importance of polyphosphate metabolism in oligotrophic environments, PLoS One, 6, e16499; DOI: 10.1371/journal.pone.0016499.PubMedCentralPubMedGoogle Scholar
  77. 77.
    McMahon, K. D., and Read, E. K. (2013) Microbial contribution to phosphorus cycling in eutrophic lakes and wastewater, Ann. Rev. Microbiol., 67, 199–219.Google Scholar
  78. 78.
    Hirota, R., Kuroda, A., Kato, J., and Ohtake, H. (2010) Bacterial phosphate metabolism and its application to phosphorus recovery and industrial bioprocesses, J. Biosci. Bioeng., 109, 423–432.PubMedGoogle Scholar
  79. 79.
    Yuan, Z., Pratt, S., and Batstone, D. J. (2012) Phosphorus recovery from wastewater through microbial processes, Curr. Opin. Biotechnol., 23, 878–883.PubMedGoogle Scholar
  80. 80.
    Gebremariam, S. Y., Beutel, M. W., Christian, D., and Hess, T. F. (2011) Research advances and challenges in the microbiology of enhanced biological phosphorus removal — a critical review, Water Environ. Res., 83, 195–219.PubMedGoogle Scholar
  81. 81.
    Fuhs, G. W., and Chen, M. (1975) Microbiological basis of phosphorus removal in the activated sludge process for the treatment of wastewaters, Microb. Ecol., 2, 119–138.PubMedGoogle Scholar
  82. 82.
    Mino, T., Kawakami, T., and Matsuo, T. (1985) Location of phosphorus in activated sludge and function of intracellular polyphosphates in biological phosphorus removal process, Water Sci. Technol., 17, 93–106.Google Scholar
  83. 83.
    Toerien, D. F., Gerber, A., Lotter, L. H., and Cloete, T. E. (1990) Enhanced phosphorus removal systems in activated sludge systems, Adv. Microb. Ecol., 11, 173–230.Google Scholar
  84. 84.
    Seviour, R. J., and Blackall, L. L. (eds.) (1999) The Microbiology of Activated Sludge, Kluwer Academic Publishing, Boston.Google Scholar
  85. 85.
    Blackall, L. L., Crocetti, G. R., Saunders, A. M., and Bond, P. L. (2002) A review and update of the microbiology of enhanced biological phosphorus removal in wastewater treatment plants, Antonie Van Leeuwenhoek, 81, 681–691.PubMedGoogle Scholar
  86. 86.
    Kortstee, G. J. J., Appeldoorn, K. J., Bonting, C. F. C., van Niel, E. W. J., and van Veen, H. W. (1994) Biology of polyphosphate accumulating bacteria, involved in enhanced biological phosphorus removal, FEMS Microbiol. Rev., 15, 137–153.PubMedGoogle Scholar
  87. 87.
    Cloete, T. E., and Oosthuizen, D. J. (2001) The role of extracellular exopolymers in the removal of phosphorus from activated sludge, Water Res., 35, 3595–3598.PubMedGoogle Scholar
  88. 88.
    Nakamura, K., Hiraishi, A., Yoshimi, Y., Kawaharasaki, M., Masuda, K., and Kamagata, Y. (1995). Microlunatus phosphovorus gen. nov. sp. nov., a new gram-positive polyphosphate-accumulating bacterium isolated from activated sludge, Int. J. System. Bacteriol., 45, 17–22.Google Scholar
  89. 89.
    Bark, K., Kampfer, P., Sponner, A., and Dott, W. (1993) Polyphosphate-dependent enzymes in some coryneform bacteria isolated from sewage sludge, FEMS Microbiol. Lett., 107, 133–138.PubMedGoogle Scholar
  90. 90.
    Erhart, R., Bradford, D., Sevior, R. J., Amann, R., and Blackall, L. L. (1997) Development and use of fluorescent in situ hybridization probes for the detection and identification of Microtrix parvicella in activated sludge, Syst. Appl. Microbiol., 20, 310–318.Google Scholar
  91. 91.
    Blackall, L. L., Crocetti, G. R., Saunders, A. M., and Bond, P. L. (2002) A review and update of the microbiology of enhanced biological phosphorus removal in waste-water treatment plants, Antonie Van Leeuwenhoek, 81, 681–691.PubMedGoogle Scholar
  92. 92.
    Maszenan, A. M., Seviour, R. J., Patel, B. K., Schumann, P., Burghardt, J., Tokiwa, Y., and Stratton, H. M. (2000) Three isolates of novel polyphosphate-accumulating gram-positive cocci, obtained from activated sludge, belong to a new genus, Tetrasphaera gen. nov., and description of two new species, Tetrasphaera japonica sp. nov. and Tetrasphaera australiensis sp. nov., Int. J. Syst. Evol. Microbiol., 50, 593–603.PubMedGoogle Scholar
  93. 93.
    Hanada, S., Liu, W. T., Shintani, T., Kamagata, Y., and Nakamura, K. (2002) Tetrasphaera elongata sp. nov., a polyphosphate-accumulating bacterium isolated from activated sludge, Int. J. Syst. Evol. Microbiol., 52, 883–887.PubMedGoogle Scholar
  94. 94.
    Zhang, H., Sekiguchi, Y., Hanada, S., Hugenholtz, P., Kim, H., Kamagata, Y., and Nakamura, K. (2003) Gemmatimonas aurantiaca gen. nov., sp. nov., a gram-negative, aerobic, polyphosphate-accumulating microorganism, the first cultured representative of the new bacterial phylum Gemmatimonadetes phyl. nov., Int. J. Syst. Evol. Microbiol., 53, 1155–1163.PubMedGoogle Scholar
  95. 95.
    Liu, W. T., Nielsen, A. T., Wu, J. H., Tsai, C. S., Matsuo, Y., and Molin, S. (2001) In situ identification of polyphosphate- and polyhydroxyalkanoate-accumulating traits for microbial populations in a biological phosphorus removal process, Environ. Microbiol., 3, 110–122.PubMedGoogle Scholar
  96. 96.
    Ashford, A. E., Vesk, P. A., Orlovich, D. A., Markovina, A. L., and Allaway, W. G. (1999) Dispersed polyphosphate in fungal vacuoles in Eucalyptus pilularis/Pisolithus tinctorius ectomycorrhizae, Fungal Genet. Biol., 28, 21–33.PubMedGoogle Scholar
  97. 97.
    Yu, T., Nassuth, A., and Peterson, R. L. (2001) Characterization of the interaction between the dark septate fungus Phialocephala fortinii and Asparagus officinalis roots, Can. J. Microbiol., 47, 741–753.PubMedGoogle Scholar
  98. 98.
    Ohtomo, R., and Saito, M. (2005) Polyphosphate dynamics in mycorrhizal roots during colonization of an arbuscular mycorrhizal fungus, New Phytologist, 167, 571–578.PubMedGoogle Scholar
  99. 99.
    Tani, C., Ohtomo, R., Osaki, M., Kuga, Y., and Ezawa, T. (2009) ATP-dependent but proton gradient-independent polyphosphate-synthesizing activity in extraradical hyphae of an arbuscular mycorrhizal fungus, Appl. Environ. Microbiol., 75, 7044–7050.PubMedCentralPubMedGoogle Scholar
  100. 100.
    Plassard, C., and Dell, B. (2010) Phosphorus nutrition of mycorrhizal trees, Tree Physiol., 30, 1129–1139.PubMedGoogle Scholar
  101. 101.
    Docampo, R., and Moreno, S. N. (2001) The acidocalcisomes, Mol. Biochem. Parasitol., 114, 151–159.PubMedGoogle Scholar
  102. 102.
    Ruiz, F. A., Lea, C. R., Oldfield, E., and Docampo, R. (2004) Human platelet dense granules contain polyphosphate and are similar to acidocalcisomes of bacteria and unicellular eukaryotes, J. Biol. Chem., 279, 44250–44257.PubMedGoogle Scholar
  103. 103.
    Omelon, S., Georgiou, J., Henneman, Z. J., Wise, L. M., Sukhu, B., Hant, T., Wynnyckyj, S., Holmyard, D., Bielecki, R., and Grynpas, M. D. (2009) Control of vertebrate skeletal mineralization by polyphosphates, PLoS ONE, 4, e5634.Google Scholar
  104. 104.
    Pavlov, E., Aschar-Sobbi, R., Campanella, M., Turner, R. J., Gomez-Garcia, M. R., and Abramov, A. Y. (2010) Inorganic polyphosphate and energy metabolism in mammalian cells, J. Biol. Chem., 285, 9420–9428.PubMedCentralPubMedGoogle Scholar
  105. 105.
    Morimoto, D., Tomita, T., Kuroda, S., Higuchi, C., Rato, S., Shiba, T., Nakagami, H., Morishita, R., and Yoshikawa, H. (2010) Inorganic polyphosphate differentiates human mesenchymal stem cells into osteoblastic cells, J. Bone Miner. Metab., 28, 418–423.PubMedGoogle Scholar
  106. 106.
    Usui, Y., Uematsu, T., Uchihashi, T., Takahashi, M., Takahashi, M., Ishizuka, M., Doto, R., Tanaka, H., Komazaki, Y., Osawa, M., Yamada, K., Yamaoka, M., and Furusawa, K. (2010) Inorganic polyphosphate induces osteoblastic differentiation, J. Dent. Res., 89, 504–509.PubMedGoogle Scholar
  107. 107.
    Muller, W. E., Wang, X., Diehl-Seifert, B., Kropf, K., Schlomacher, U., Lieberwirth, I., Glasser, G., Wiens, M., and Schroder, H. C. (2011) Inorganic polymeric phosphate/polyphosphate as an inducer of alkaline phosphatase and a modulator of intracellular Ca(2+) level in osteoblasts (SaOS-2 cells) in vitro, Acta Biomater., 7, 2661–2671.PubMedGoogle Scholar
  108. 108.
    Smith, S. A., Mutch, N. J., Baskar, D., Rohloff, P., Docampo, R., and Morrissey, J. H. (2006) Polyphosphate modulates blood coagulation and fibrinolysis, Proc. Natl. Acad. Sci. USA, 103, 903–908.PubMedCentralPubMedGoogle Scholar
  109. 109.
    Smith, S. A., and Morrissey, J. H. (2008) Polyphosphate as a general procoagulant agent, J. Thromb. Haemost., 6, 1750–1756.PubMedCentralPubMedGoogle Scholar
  110. 110.
    Smith, S. A., Choi, S. H., Davis-Harrison, R., Huyck, J., Boettcher, J., Reinstra, C. M., and Morrissey, J. H. (2010) Polyphosphate exerts differential effects on blood clotting, depending on polymer size, Blood, 116, 4353–4359.PubMedCentralPubMedGoogle Scholar
  111. 111.
    Van der Meijden, P. E., and Heemskerk, J. W. (2010) Polyphosphates: a link between platelet activation, intrinsic coagulation and inflammation? Expert Rev. Hematol., 3, 269–272.PubMedGoogle Scholar
  112. 112.
    Mackman, N., and Gruber, A. (2010) Platelet polyphosphate: an endogenous activator of coagulation factor XII, J. Thromb. Haemost., 8, 865–867.PubMedCentralPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  • T. V. Kulakovskaya
    • 1
    Email author
  • L. P. Lichko
    • 1
  • L. P. Ryazanova
    • 1
  1. 1.Skryabin Institute of Biochemistry and Physiology of MicroorganismsRussian Academy of SciencesPushchino, Moscow RegionRussia

Personalised recommendations