Skip to main content
SpringerLink
Log in

Role of Phosphate-Accumulating Bacteria in Biological Phosphorus Removal from Wastewater

  • Published:
Applied Biochemistry and Microbiology Aims and scope Submit manuscript

Abstract

The review examines the microbiological aspects of the biological phosphorus removal from wastewater. The history of the development of biotechnology and the discovery of the physiological group of phosphate-accumulating organisms (PAOs), which biologically remove phosphorus via the phosphate uptake and storage in the form of intracellular polyphosphates, is briefly described. PAOs are characterized by a cyclic type of metabolism that occurs when the anaerobic/aerobic conditions cyclically change. Under anaerobic conditions, PAOs uptake and store organic compounds through the energy of degradation of intracellular polyphosphates. When anaerobic conditions change to aerobic or an alternative electron acceptor appears, PAOs uptake phosphates and synthesize intracellular polyphosphates using the intracellular polymeric sources of carbon and energy accumulated under anaerobic conditions. The main representatives of the PAOs, their metabolic models, and physiological characteristics are described. The basic principles of the implementation of biotechnology used in the practice of wastewater treatment for phosphorus and other nutrients are considered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5
Fig. 6.

Similar content being viewed by others

REFERENCES

  1. Farley, M., Eutrophication in fresh waters: an international review, inEncyclopedia of Lakes and Reservoirs, Bengtsson, L. and Herschy, R.W., Eds., New York: Fairbridge Springer-Verlag Inc., 2012, pp. 258–270.

    Google Scholar 

  2. Cordell, D. and White, S., Agronomy, 2013, vol. 3, pp. 86–116. https://doi.org/10.3390/agronomy3010086

    Article  Google Scholar 

  3. Cornel, P. and Schaum, C., Water Sci. Technol., 2009, vol. 59, no. 6, pp. 1069–1076.

    Article  CAS  PubMed  Google Scholar 

  4. Phosphorus and Nitrogen Removal from Municipal Wastewater Principles and Practices, 2nd ed., Sedlak, R.I., Ed., CRC Press, Taylor and Frances Group, 1991.

    Google Scholar 

  5. Bunce, J.T., Ndam, E., Ofiteru, I.D., Moore, A., and Graham, D.W., Front. Environ. Sci., 2018, vol. 6, article 8. https://doi.org/10.3389/fenvs.2018.00008

    Article  Google Scholar 

  6. Hirota, R., Kuroda, A., Kato, J., and Ohtake, H., J. Biosci. Bioeng., 2010, vol. 109, no. 5, pp. 423–432.

    Article  CAS  PubMed  Google Scholar 

  7. Wilfert, P., Kumar, P.S., Korving, L., Witkamp, G.-J., and van Loosdrecht, M.C.M., Environ. Sci. Technol., 2015, vol. 49, no. 16, pp. 9400–9414.

    Article  CAS  PubMed  Google Scholar 

  8. Srinath, E.G., Sastry, C.A., and Pillai, S.C., Experientia, 1959, vol. 15, no. 9, pp. 339–340.

    Article  CAS  PubMed  Google Scholar 

  9. Shapiro, J., Levin, G.V., and Zea, H.G., J. Water Pollut. Control Fed., 1967, vol. 39, no. 11, pp. 1811–1818.

    Google Scholar 

  10. Shapiro, J., Science, 1967, vol. 155, pp. 1269–1271.

    Article  CAS  PubMed  Google Scholar 

  11. Barnard, J.L., Water Wastes Eng., 1974, vol. 11, no. 7, pp. 33–36.

    CAS  Google Scholar 

  12. Barnard, J.L., Water Res., 1975, vol. 9, nos. 5–6, pp. 485–490.

    Article  CAS  Google Scholar 

  13. Nicholls, H.A., Water SA, 1975, vol. 1, no. 3, pp. 121–132.

    CAS  Google Scholar 

  14. Janssen, P.M.J., Meinema, K., and van der Roes, H.F., Biological Phosphorus Removal: Manual for Design and Operation, London: Stowa, 2002.

    Google Scholar 

  15. Wentzel, M.C. and Comeau, Y., Enhanced biological nutrient removal, in Biological Wastewater Treatment Principles, Modelling and Design, Henze, M., van Loosdrecht, M.C.M., Ekama, G.A., and Brdjanovic, D., Eds., London: IWA Publ., 2008, pp. 155–220.

    Google Scholar 

  16. Levin, G.V. and Shapiro, J., J. Water Pollut. Control Fed., 1965, vol. 37, no. 6, pp. 800–821.

    CAS  Google Scholar 

  17. Fuhs, G.W. and Chen, M., Microbiol. Ecol., 1975, vol. 2, no. 2, pp. 119–138.

    Article  CAS  Google Scholar 

  18. Kulaev, I.S., Vagabov, V.M., and Kulakovskaya, T.V., The Biochemistry of Inorganic Polyphosphates, 2nd ed., Wiley, 2004.

    Book  Google Scholar 

  19. Rehm, B.H.A., Nat. Rev. Microbiol., 2010, vol. 8, no. 8, pp. 578–592.

    Article  CAS  PubMed  Google Scholar 

  20. Wentzel, M.C., Loewenthal, R.E., Ekama, G.A., and Marais, G.V.R., Water S.A., 1988, vol. 14, no. 2, pp. 81–92.

    CAS  Google Scholar 

  21. Schuler, A.J. and Jenkins, D., Water Environ. Res., 2003, vol. 75, no. 6, pp. 485–498.

    Article  CAS  PubMed  Google Scholar 

  22. Welles, L., Abbas, B., Sorokin, D.Y., Lopez-Vazquez, C.M., Hooijmans, C.M., van Loosdrecht, M.C.M., and Brdjanovic, D., Front. Microbiol., 2016, vol. 7, p. 2121. https://doi.org/10.3389/fmicb.2016.02121

    Article  PubMed  Google Scholar 

  23. Van Loosdrecht, M.C.M., Hooijmans, C.M., Brdjanovic, D., and Heijnen, J.J., Appl. Microbiol. Biotechnol., 1997, vol. 48, no. 2, pp. 289–296.

    Article  CAS  Google Scholar 

  24. Mino, T., Van Loosdrecht, M.C.M., and Heijnen, J.J., Wat. Res, 1998, vol. 32, no. 11, pp. 3193–3207.

    Article  CAS  Google Scholar 

  25. Seviour, R.J., Mino, T., and Onuki, M., FEMS Microbiol. Rev., 2003, vol. 27, no. 1, pp. 99–127.

    Article  CAS  PubMed  Google Scholar 

  26. Dorofeev, A.G., Nikolaev, Yu.A., Mardanov, A.V., and Pimenov, N.V., Microbiology (Moscow), 2019, vol. 88, no. 4, pp. 402–415.

    Article  CAS  Google Scholar 

  27. Mino, T., Arun, V., Tsuzuki, Y., and Matsuo, T., Effect of phosphorus accumulation on acetate metabolism in the biological phosphorus removal, in Biological Phosphate Removal from Wastewaters, Ramadori, R., Ed., Oxford: Pergamon Press, 1987, pp. 27–38.

    Google Scholar 

  28. Arun, V., Mino, T., and Matsuo, T., Water Res., 1988, vol. 22, no. 5, pp. 565–570.

    Article  CAS  Google Scholar 

  29. Comeau, Y., Hall, K.J., Hancock, R.E.W., and Oldham, W.K., Water Res., 1986, vol. 20, no. 12, pp. 1511–1521.

    Article  CAS  Google Scholar 

  30. Wentzel, M.C., Lotter, L.H., Loewenthal, R.E., and Marais, G.V.R., Water S.A., 1986, vol. 12, no. 4, pp. 209–224.

    CAS  Google Scholar 

  31. Hesselmann R.P.X., Von Rummell, R., Resnick, S.M., Hany, R., and Zehnder, J.B., Water Res., 2000, vol. 34, no. 14, pp. 3487–3494.

    Article  CAS  Google Scholar 

  32. Pijuan, M., Oehmen, A., Baeza, J.A., Casas, C., and Yuan, Z., Biotechnol. Bioeng., 2008, vol. 99, no. 1, pp. 170–179.

    Article  CAS  PubMed  Google Scholar 

  33. Hesselmann, R.P.X., Werlen, C., Hahn, D., van der Meer, J.R., and Zehnder, A.J.B., Syst. Appl. Microbiol., 1999, vol. 22, pp. 454–465.

    Article  CAS  PubMed  Google Scholar 

  34. Bond, P.L., Hugenholtz, P., Keller, J., and Blackall, L.L., Appl. Environ. Microbiol., 1995, vol. 61, no. 5, pp. 1910–1916.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Crocetti, G.R., Hugenholtz, P., Bond, P.L., Schuler, A., Keller, J., Jenkins, D., and Blackall, L.L., Appl. Environ. Microbiol., 2000, vol. 66, no. 3, pp. 1175–1182.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zilles, J.L., Peccia, J., Kim, M., Hung, C., and Noguera, D.R., Appl. Environ. Microbiol., 2002, vol. 68, no. 6, pp. 2763–2769.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Zilles, J.L., Hung, C.H., and Noguera, D.R., Water Sci. Technol., 2002, vol. 46, nos. 1–2, pp. 123–128.

    Article  CAS  PubMed  Google Scholar 

  38. Kong, Y.H., Nielsen, J.L., and Nielsen, P.H., Appl. Environ. Microbiol., 2004, vol. 70, no. 9, pp. 5383–5390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. He, S., Gu, A.Z., and McMahon, K.D., Microb. Ecol., 2008, vol. 55, no. 2, pp. 229–236.

    Article  PubMed  Google Scholar 

  40. Lu, H., Oehmen, A., Virdis, B., Keller, J., and Yuan, Z., Water Res., 2006, vol. 40, no. 20, pp. 3838–3848.

    Article  CAS  PubMed  Google Scholar 

  41. Peterson, S.B., Warnecke, F., Madejska, J., McMahon, K.D., and Hugenholtz, P., Environ. Microbiol., 2008, vol. 10, no. 10, pp. 2692–2703.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. McMahon, K.D., Dojka, M.A., Pace, N.R., Jenkins, D., and Keasling, J.D., Appl. Environ. Microbiol., 2002, vol. 68, no. 10, pp. 4971–4978.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. He, S., Gall, D.L., and McMahon, K.D., Appl. Environ. Microbiol., 2007, vol. 73, no. 18, pp. 5865–5874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kim, J.M., Lee, H.J., Kim, S.Y., Song, J.J., Park, W., and Jeon, C.O., Appl. Environ. Microbiol., 2010, vol. 76, no. 12, pp. 3825–3835.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Mao, Y., Graham, D.W., Tamaki, H., and Zhang, T., Sci. Rep., 2015, vol. 5, p. 11857. https://www.nature. com/articles/srep11857.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Martin, G.H., Ivanova, N., Kunin, V., Warnecke, F., Barry, K.W., McHardy, A.C., Yeates, C., He, S., Salamov, A.A., Szeto, E., Dalin, E., Putnam, N.H., Shapiro, H.J., Pangilinan, J.L., Rigoutsos, I., Kyrpides, N.C., Blackall, L.L., McMahon, K.D., and Hugenholtz, P., Nat. Biotechnol., 2006, vol. 24, no. 10, pp. 1263–1269.

    Article  CAS  Google Scholar 

  47. Mino, T. and Satoh, H., Nat. Biotechnol., 2006, vol. 24, no. 10, pp. 1229–1230.

    Article  CAS  PubMed  Google Scholar 

  48. He, S. and McMahon, K.D., Microb. Biotechnol., 2011, vol. 4, no. 5, pp. 603–619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Flowers, J.J., He, S., Malfatti, S., del Rio, T.G., Tringe, S.G., Hugenholtz, P., and McMahon, K.D., ISME J., 2013, vol. 7, no. 12, pp. 2301–2314.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Wexler, M., Richardson, D.J., and Bond, P.L., Environ. Microbiol., 2009, vol. 11, no. 12, pp. 3029–3044.

    Article  CAS  PubMed  Google Scholar 

  51. Skennerton, C.T., Barr, J.J., Slater, F.R., Bond, P.L., and Tyson, G.W., Environ. Microbiol., 2015, vol. 17, no. 5, pp. 1574–1585.

    Article  CAS  PubMed  Google Scholar 

  52. Wilmes, P., Andersson, A.F., Lefsrud, M.G., Wexler, M., Shah, M., Zhang, B., Hettich, R.L., Bond, P.L., Verberkmoes, N.C., and Banfield, J.F., ISME J., 2008, vol. 2, pp. 853–864.

    Article  CAS  PubMed  Google Scholar 

  53. Oyserman, B.O., Noguera, D.R., del Rio, T.G., Tringe, S.G., and McMahon, K.D., ISME J., 2016, vol. 10, no. 4, pp. 810–822.

    Article  CAS  PubMed  Google Scholar 

  54. Wong, M.T., Mino, T., Seviour, R.J., Onuki, M., and Liu, W.-T., Water Res., 2005, vol. 39, no. 13, pp. 2901–2914.

    Article  CAS  PubMed  Google Scholar 

  55. Beer, M., Stratton, H.M., Griffiths, P.C., and Seviour, R.J., J. Appl. Microbiol., 2006, vol. 100, no. 1, pp. 223–243.

    Article  CAS  Google Scholar 

  56. Nguyen, H.T., Nielsen, J.L., and Nielsen, P.H., Environ. Microbiol., 2012, vol. 14, no. 10, pp. 2826–2837.

    Article  CAS  PubMed  Google Scholar 

  57. Tarayre, C., Nguyen, H.-T., Brognaux, A., Delepierre, A., De Clercq, L., Charlier, R., Michels, E., Meers, E., and Delvigne, F., Sensors, 2016, vol. 16, pp. 1–14.

    Article  Google Scholar 

  58. Stokholm-Bjerregaard, M., McIlroy, S.J., Nierychlo, M., Karst, S.M., Albertsen, M., and Nielsen, P.H.A., Front. Microbiol., 2017, vol. 8, p. 718. https://doi.org/10.3389/fmicb.2017.00718

    Article  PubMed  PubMed Central  Google Scholar 

  59. Tarayre, C., Charlier, R., Delepierre, A., Brognaux, A., Bauwens, J., Francis, F., Dermience, M., Lognay, G., Taminiau, B., Daube, G., Compere, P., Meers, E., Michels, E., and Delvigne, F., Environ. Sci. Pollut. Res., 2017, vol. 24, no. 9, pp. 8017–8032.

    Article  CAS  Google Scholar 

  60. Maszenan, A.M., Seviour, R.J., Patel, B.K.C., Schumann, P., Burghardt, J., Tokiwa, Y., and Stratton, H.M., Int. J. Syst. Evol. Microbiol., 2000, vol. 50, no. 2, pp. 593–603.

    Article  CAS  PubMed  Google Scholar 

  61. Kong, Y., Nielsen, J.L., and Nielsen, P.H., Appl. Environ. Microbiol., 2005, vol. 71, no. 7, pp. 4076–4085.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Nguyen, H.T., Le, V.Q., Hansen, A.A., Nielsen, J.L., and Nielsen, P.H., FEMS Microbiol. Ecol., 2011, vol. 76, no. 2, pp. 256–267.

    Article  CAS  PubMed  Google Scholar 

  63. Muszynski, A. and Zaleska-Radziwill, M., Archit. Civ. Eng. Environ., 2015, vol. 8, no. 4, pp. 99–105.

    Google Scholar 

  64. Kong, Y., Xia, Y., and Nielsen, P.H., Environ. Microbiol., 2008, vol. 10, no. 8, pp. 2008–2019.

    Article  CAS  PubMed  Google Scholar 

  65. Nielsen, J.L., Nguyen, H., Meyer, R.L., and Nielsen, P.H., Microbiology, 2012, vol. 158, pp. 1818–1825.

    Article  CAS  PubMed  Google Scholar 

  66. Kristiansen, R., Nguyen, H.T.T., Saunders, A.M., Nielsen, J.L., Wimmer, R., Le, V.Q., McIlroy, S.J., Petrovski, S., Seviour, R.J., Calteau, A., Nielsen, K.L., and Nielsen, P.H., ISME J., 2013, vol. 7, pp. 543–554.

    Article  CAS  PubMed  Google Scholar 

  67. Nguyen, H.T., Kristiansen, R., Vestergaard, M., Wimmer, R., and Nielsen, P.H., Appl. Environ. Microbiol., 2015, vol. 81, no. 14, pp. 4809–4818.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Hanada, S., Liu, W.T., Shintani, T., Kamagata, Y., and Nakamura, K., Int. J. Syst. Evol. Microbiol., 2002, vol. 52, pp. 883–887.

    CAS  PubMed  Google Scholar 

  69. Onda, S. and Takii, S., J. Gen. Appl. Microbiol., 2002, vol. 48, pp. 125–133.

    Article  CAS  PubMed  Google Scholar 

  70. McKenzie, C.M., Seviour, E.M., Schumann, P., Maszenan, A.M., Liu, J.-R., Webb, R.I., Monis, P., Saint, C.P., Steiner, U., and Seviour, R.J., Int. J. Syst. Evol. Microbiol., 2006, vol. 56, pp. 2279–2290.

    Article  CAS  PubMed  Google Scholar 

  71. Nakamura, K., Hiraishi, A., Yoshimi, Y., Kawaharasaki, M., Masuda, K., and Kamagata, Y., Int. J. Syst. Bacteriol., 1995, vol. 45, pp. 17–22.

    Article  CAS  PubMed  Google Scholar 

  72. Kawakoshi, A., Nakazawa, H., Fukada, J., Sasagawa, M., Katano, Y., Nakamura, S., Hosoyama, A., Sasaki, H., Ichikawa, N., Hanada, S., K-amagata, Y., Nakamura, K., Yamazaki, S., and Fujita, N., DNA Res., 2012, vol. 19, no. 5, pp. 383–394.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Nakamura, K., Masuda, K., and Mikami, E., J. Ferment. Bioeng., 1991, vol. 4, pp. 258–263.

    Article  Google Scholar 

  74. Marques, R., Santos, J., Nguyen, H., Carvalho, G., Noronha, J.P., Nielsen, P.H., Reis, M.A.M., and Oehmen, A., Water Res., 2017, vol. 122, pp. 159–171.

    Article  CAS  PubMed  Google Scholar 

  75. Chernousova, E., Gridneva, E., Grabovich, M., Dubinina, G., Akimov, V., Rossetti, S., and Kuever, J., Int. J. Syst. Evol. Microbiol., 2009, vol. 59, no. 12, pp. 3128–3135.

    Article  CAS  PubMed  Google Scholar 

  76. Rubio-Rincón, F.J., Welles, L., Lopez-Vazquez, C.M., Nierychlo, M., Abbas, B., Geleijnse, M., Nielsen, P.H., van Loosdrecht, M.C.M., and Brdjanovic, D., Water Res., 2017, vol. 116, pp. 53–64.

    Article  CAS  PubMed  Google Scholar 

  77. Kong, Y., Xia, Y., Nielsen, J.L., and Nielsen, P.H., Microbiology, 2007, vol. 153, no. 12, pp. 4061–4073.

    Article  CAS  PubMed  Google Scholar 

  78. Terashima, M., Yama, A., Sato, M., Yumoto, I., Kamagata, Y., and Kato, S., Microbes Environ., 2016, vol. 31, no. 4, pp. 449–455.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Zhang, H., Sekiguchi, Y., Hanada, S., Hugenholtz, P., Kim, H., Kamagata, Y., and Nakamura, K., Int. J. Syst. Evol. Microbiol., 2003, vol. 53, pp. 1155–1163.

    Article  CAS  PubMed  Google Scholar 

  80. Spring, S., Wagner, M., Schumann, P., and Kampfer, P., Int. J. Syst. Evol. Microbiol., 2005, vol. 55, pp. 621–629.

    Article  CAS  PubMed  Google Scholar 

  81. Sun, L., Zhao, X., Zhang, H., and Zhang, Y., Ecol. Eng., 2015, vol. 81, pp. 82–88.

    Article  Google Scholar 

  82. Soo, R.M., Skennerton, C.T., Sekiguchi, Y., Imelfort, M., Paech, S.J., Dennis, P.G., Steen, J.A., Parks, D.H., Tyson, G.W., and Hugenholtz, P.,Genome Biol. Evol., 2014, vol. 6, pp. 1031–1045.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Welles, L., Tian, W.D., Saad, S., Abbas, B., Lopez-Vazquez, C.M., Hooijmans, C.M., van Loosdrecht, M.C.M., and Brdjanovic, D., Water Res., 2015, vol. 83, pp. 354–366.

    Article  CAS  PubMed  Google Scholar 

  84. Smolders, G.J.F., Van der Meij, J., Van Loosdrecht, M.C.M., and Heijnen, J.J., Biotechnol. Bioeng., 1994, vol. 43, no. 6, pp. 461–470.

    Article  CAS  PubMed  Google Scholar 

  85. Nakamura, K., Ishikawa, S., and Kawaharasaki, M., J. Ferment. Bioeng., 1995, vol. 80, pp. 377–382.

    Article  CAS  Google Scholar 

  86. Smolders, G.J.F., van Loosdrccht, M.C.M., and Heijnen, J.J., Biotechnol. Bioeng., 1994, vol. 44, no. 7, pp. 837–848.

    Article  CAS  PubMed  Google Scholar 

  87. Henze, M., Harremoes, P., Jansen, J.C., and Arvin, E., Wastewater Treatment: Biological and Chemical Processes, Berlin: Springer-Verlag, 1997.

    Book  Google Scholar 

  88. Mino, T., Liu, W.-T., Kurisu, F., and Matsuo, T., Water Sci. Technol., 1995, vol. 31, no. 2, pp. 25–34.

    Article  CAS  Google Scholar 

  89. McMahon, K.D., He, S., and Oehmen, A., The microbiology of phosphorus removal, in The Microbiology of Phosphorus Removal. Microbial Ecology of Activated Sludge, Seviour, R. and Nielsen, P.H., Eds., London: IWA, 2010, pp. 281–319.

    Google Scholar 

  90. Brdjanovic, D., Logemann, S., Van Loosdrecht, M.C.M., Hooijmans, C.M., Alaerts, G.J., and Heijnen, J.J., Water Res., 1998, vol. 32, no. 4, pp. 1035–1048.

    Article  CAS  Google Scholar 

  91. Helmer, C. and Kunst, S., Water Sci. Technol., 1998, vol. 37, nos. 4–5, pp. 531–539.

    Article  CAS  Google Scholar 

  92. Erdal, U.G., Erdal, Z.K., and Randall, C.W., Water Sci. Technol., 2003, vol. 47, no. 11, pp. 1–8.

    Article  CAS  PubMed  Google Scholar 

  93. Panswad, T., Doungchai, A., and Anotai, J., Water Res., 2003, vol. 37, pp. 409–415.

    Article  CAS  PubMed  Google Scholar 

  94. Zheng, X., Sun, P., Han, J., Song, Y., Hu, Z., Fan, H., and Lv, S., Proc. Biochem. Soc., 2014, vol. 49, no. 12, pp. 2207–2213.

    Article  CAS  Google Scholar 

  95. Tian, W., Lopez-Vazquez, C.M., Li, W., Brdjanovic, D., and van Loosdrecht, M.C.M., Chemosphere, 2013, vol. 92, no. 10, pp. 1314–1320.

    Article  CAS  PubMed  Google Scholar 

  96. Brdjanovic, D., van Loosdrecht, M.C.M., Hooijmans, C.M., Alaerts, G.J., and Heijnen, J.J., ASCE J. Environ. Eng., 1997, vol. 123, no. 2, pp. 144–154.

    Article  CAS  Google Scholar 

  97. Lopez-Vazquez, C.M., Song, Y.I., Hooijmans, C.M., Brdjanovic, D., Moussa, M.S., Gijzen, H.J., and van Loosdrecht, M.M., Biotechnol. Bioeng., 2007, vol. 97, no. 3, pp. 483–495.

    Article  CAS  PubMed  Google Scholar 

  98. Ong, Y.H., Chua, A.S.M., Huang, Y.N., Ngoh, G.C., and You, S.J., SustainableEnviron. Res., 2016, vol. 26, pp. 14–19.

    CAS  Google Scholar 

  99. Ong, Y.H., Chua, A.S.M., Lee, B.P., and Ngoh, G.C., Water Sci. Technol., 2013, vol. 67, no. 2, pp. 340–346.

    Article  CAS  PubMed  Google Scholar 

  100. Cao, Y., Kwok, B.H., van Loosdrecht, M.C., Daigger, G.T., Png, H.Y., Long, W.Y., Chye, C.S., and Ghani, Y.A., Water Sci. Technol., 2017, vol. 75, nos. 3–4, pp. 741–751.

    Article  CAS  PubMed  Google Scholar 

  101. Law, Y., Kirkegaard, R.H., Cokro, A.A., Liu, X., Arumugam, K., Xie, C., Stokholm-Bjerregaard, M., Drautz-Moses, D.I., Nielsen, P.H., Wuertz, S., and Williams, R.B.H., Sci. Rep., 2016, vol. 6, article 25719. https://doi.org/10.1038/srep25719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Qiu, G., Zuniga-Montanez, R., Law, Y., Thi, S.S., Nguyen, T.Q.N., Eganathan, K., Liu, X., Nielsen, P.H., Williams, R.B.H., and Wuertz, S., Water Res., 2019, vol. 149, pp. 496–510.

    Article  CAS  PubMed  Google Scholar 

  103. Ong, Y.H., Chua, A.S.M., Fukushima, T., Ngoh, G.C., Shoji, T., and Michinaka, A., Water Res., 2014, vol. 64, pp. 102–112.

    Article  CAS  PubMed  Google Scholar 

  104. Shen, N., Chen, Y., and Zhou, Y., Water Res., 2017, vol. 114, pp. 308–315.

    Article  CAS  PubMed  Google Scholar 

  105. Kuba, T., Murnleitner, E., van Loosdrecht, M.C.M., and Heijnen, J.J., Biotechnol. Bioeng., 1996, vol. 52, no. 6, pp. 685–695.

    Article  CAS  PubMed  Google Scholar 

  106. Kuba, T., Van Loosdrecht, M.C.M., and Heijnen, J., Water Res., 1996, vol. 30, no. 7, pp. 1702–1710.

    Article  CAS  Google Scholar 

  107. Lanham, A.B., Oehmen, A., Carvalho, G., Saunders, A.M., Nielsen, P.H., and Reis, M.A.M., Water Sci. Technol., 2018, vol. 78, no. 12, pp. 2449–2458.

    Article  CAS  PubMed  Google Scholar 

  108. Zou, H. and Wang, Y., Environ. Protect. Eng., 2017, vol. 43, no. 3, pp. 225–237.

    Google Scholar 

  109. Flowers, J.J., He, S., Yilmaz, S., Noguera, D.R., and McMahon, K.D., Environ. Microbiol. Rep., 2009, vol. 1, no. 6, pp. 583–588.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Lanham, A.B., Moita, R., Lemos, P.C., and Reis, M.A.M., Water Sci. Technol., 2011, vol. 63, no. 2, pp. 352–359.

    Article  CAS  PubMed  Google Scholar 

  111. Rubio-Rincón, F.J., Lopez-Vazquez, C.M., Welles, L., van Loosdrecht, M.C.M., and Brdjanovic, D., Water Res., 2017, vol. 120, pp. 156–164.

    Article  CAS  PubMed  Google Scholar 

  112. Saad, S., Welles, L., Abbas, B., Lopez-Vazquez, C., van Loosdrecht, M., and Brdjanovic, D., Water Res., 2016, vol. 105, pp. 97–109.

    Article  CAS  PubMed  Google Scholar 

  113. Marques, R., Ribera-Guardia, A., Santos, J., Carvalho, G., Reis, M.A.M., Pijuan, M., and Oehmen, A., Water Res., 2017, vol. 137, pp. 262–272.

    Article  CAS  Google Scholar 

  114. Zeng, W., Li, B., Wang, X., Bai, X., and Peng, Y., Chemosphere, 2016, vol. 144, pp. 1018–1025.

    Article  CAS  PubMed  Google Scholar 

  115. Meinhold, J., Arnold, E., and Isaacs, S., Water Res., 1999, vol. 33, pp. 1871–1883.

    Article  CAS  Google Scholar 

  116. Saito, T., Brdjanovic, D., and Van Loosdrecht, M.C.M., Water Res., 2004, vol. 38, pp. 3760–3768.

    Article  CAS  PubMed  Google Scholar 

  117. Pijuan, M., Ye, L., and Yuan, Z., Water Res., 2010, vol. 44, pp. 6063–6072.

    Article  CAS  PubMed  Google Scholar 

  118. Zhoy, Y., Ganda, L., Lim, M., Yuan, Z., and Ng, W.J., Bioresour. Technol., 2012, vol. 116, pp. 340–347.

    Article  CAS  Google Scholar 

  119. Zhou, Y., Pijuan, M., and Yuan, Z., Biotechnol. Bioeng., 2007, vol. 98, pp. 903–912.

    Article  CAS  PubMed  Google Scholar 

  120. Zhou, Y., Ganda, L., Lim, M., Yuan, Z., Kjelleberg, S., and Ng, W., Appl. Micobiol. Biotechnol., 2010, vol. 88, pp. 359–369.

    Article  CAS  Google Scholar 

  121. Ye, L., Pijuan, M., and Yuan, Z., Bioresour. Technol., 2013, vol. 130, pp. 382–389.

    Article  CAS  PubMed  Google Scholar 

  122. Welles, L., Lopez-Vazquez, C.M., Hooijmans, C.M., van Loosdrecht, M.C.M., and Brdjanovic, D., AMB Express, 2016, p. 6, p. 44. https://doi.org/10.1186/s13568-016-0214-z

  123. Nurmiyanto, A., Kodera, H., Kindaichi, T., Ozaki, N., Aoi, Y., and Ohashi, A., Microbes Environ., 2017, vol. 32, no. 3, pp. 260–267.

    Article  PubMed  PubMed Central  Google Scholar 

  124. Dorofeev, A.G., Grigor’eva, N.V., Kozlov, M.N., Kevbrina, M.V., Aseeva, V.G., and Nikolaev, Yu.A., Microbiology (Moscow), 2014, vol. 83, no. 5, pp. 450–461.

    Article  CAS  Google Scholar 

  125. Tchobanoglous, G., Burton, F.L., and Stensel, H.D., Wastewater Engineering: Treatment and Reuse, McGraw Hill, New York, USA: Metcalf and Eddy, 2014.

  126. Sequencing Batch Reactor Technology, Scientific and Technical Reports no. 10, Wilderer, P.A., Irvine, R.L., and Goronszy, M.C., IWA Publishing, 2001.

  127. Artan, N. and Orhon, D., Mechanism and Design of Sequencing Batch Reactors for Nutrient Removal, Scientific and Technical Report Series, no. 19, London: Iwa Publishing, 2005.

  128. Saad, A.S., Welles, L., Lopez, C.M., van Loosdrecht, M.C.M., and Brdjanovic, D., Chem. Eng. J., 2017, vol. 326, pp. 68–77.

    Article  CAS  Google Scholar 

  129. Von Sperling, M., Activated Sludge and Aerobic Biofilm Reactors, vol. 8 of Biological Wastewater Treatment, London: IWA Publishing, 2007.

  130. Wang, L.K. and Li, Y., Sequencing Batch Reactors Handbook of Environmental Engineering Series, vol. 8: Biological Treatment Processes, Wang, L.K., Pereira, N.C., Hung, Y.T., and Shammas, N.K., Eds., Humana Press, 2009, pp. 459–511.

  131. Barnard, J. and Comeau, Y., Phosphorus removal in activated sludge, in Activated Sludge—100 Years and Counting, Jenkins, D. and Wanner, J., Eds., IWA Publishing, 2014, pp. 93–115.

    Google Scholar 

  132. Neethling, J.B., Bakke, B., Benisch, M., Gu, A., Stephens, H., Stensel, H.D., and Moore, R., Factors Influencing the Reliability of Enhanced Biological Phosphorus Removal, WERF Report 01-CTS-3, London: IWA, 2005

  133. Barnard, J.L., Water S.A., 1976, vol. 2, no. 3, pp. 136–144.

    CAS  Google Scholar 

  134. Marais, G.V.R., Loewenthal, R.E., and Siebritz, I.P., Water Sci. Technol., 1983, vol. 15, no. 3, pp. 15–41.

    Article  CAS  Google Scholar 

  135. Wang, D.B., Li, X.M., Yang, Q., Zeng, G.M., Liao, D.X., and Zhang, J., Bioresour. Technol., 2008, vol. 99, pp. 5466–5473.

    Article  CAS  PubMed  Google Scholar 

  136. Chen, H.B., Wang, D.B., Li, X.M., Yang, Q., Luo, K., Zeng, G., Tang, M., Xiong, W., and Yang, G., Biochem. Eng. J., 2014, vol. 90, pp. 27–35.

    Article  CAS  Google Scholar 

  137. Wang, D., Xu, Q., Yang, W., Chen, Y., Li, X., Liao, D., Yang, G., Yang, Q., and Zeng, G., Biochem. Eng. J., 2014, vol. 87, pp. 15–24.

    Article  CAS  Google Scholar 

  138. Wang, D., Li, X., Yang, Q., Zheng, W., Liu, Z., Liu, Y., Cao, J., Yue, X., Shen, T., Zeng, G., and Deng, J., Bioresour. Technol., 2009, vol. 100, pp. 4005–4011.

    Article  CAS  PubMed  Google Scholar 

  139. Guo, G., Wu, D., Ekama, G.A., Hao, T., Mackey, H.A., and Chen, G., Water Res., 2018, vol. 141, pp. 9–18.

    Article  CAS  PubMed  Google Scholar 

  140. Oyserman, B.O., Martirano, J.M., Wipperfurth, S., Owen, B.R., Noguera, D.R., and McMahon, K.D., Environ. Sci. Technol., 2017, vol. 51, no. 6, pp. 3165–3175.

    Article  CAS  PubMed  Google Scholar 

  141. De Almeida, L.G., Ortiz, J.H., Schneider, R.P., and Spira, B., Appl. Environ. Microbiol., 2015, vol. 81, no. 9, pp. 3006–3015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Zhou, Y., Lisowski, W., Zhou, Y., Jern, N.W., Huang, K., and Fong, E., Biotechnol. Lett., 2017, vol. 39, no. 10, pp. 1509–1514. https://doi.org/10.1007/s10529-017-2383-5

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The work was funded by Russian Foundation for Basic Research (project no. 18-29-25016MK) and by the Ministry of Science and Higher Education of the Russian Federation.

Author information

Authors and Affiliations

  1. Winogradsky Institute of Microbiology, Fundamentals of Biotechnology Federal Research Center, Russian Academy of Sciences, 119071, Moscow, Russia

    A. G. Dorofeev, Yu. A. Nikolaev & N. V. Pimenov

  2. OJSC Moswodikanal, 105005, Moscow, Russia

    A. G. Dorofeev

  3. Bioengineering Center, Fundamentals of Biotechnology Federal Research Center, Russian Academy of Sciences, 119071, Moscow, Russia

    A. V. Mardanov

Authors
  1. A. G. Dorofeev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu. A. Nikolaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. V. Mardanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. V. Pimenov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. G. Dorofeev.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by A. Bulaev

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dorofeev, A.G., Nikolaev, Y.A., Mardanov, A.V. et al. Role of Phosphate-Accumulating Bacteria in Biological Phosphorus Removal from Wastewater. Appl Biochem Microbiol 56, 1–14 (2020). https://doi.org/10.1134/S0003683820010056

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0003683820010056

Keywords:

Search

Navigation