Hydrobiologia

, Volume 170, Issue 1, pp 157–175 | Cite as

Phosphatases; origin, characteristics and function in lakes

  • Mats Jansson
  • Håkan Olsson
  • Kurt Pettersson
Article

Abstract

Phosphatases catalyze the liberation of orthophosphate from organic phosphorus compounds. The total phosphatase activity in lake water results from a mixture of phosphatases localized on the cell surfaces of algae and bacteria and from dissolved enzymes supplied by autolysis or excretion from algae, bacteria and zooplankton. External lake water phosphatases usually have pH optima in the alkaline region. Acid phosphatases generally seem to be active in the internal cell metabolism. The synthesis of external alkaline phosphatases is often repressed at high phosphate concentrations and derepressed at low phosphate concentrations. Phosphatase activity has therefore been used as a phosphorus deficiency indicator in algae and in natural plankton populations. The possibilities for this interpretation of phosphatase activity in lake water are limited, however, and this is discussed. The in situ hydrolysis capacity, i.e. the rate by which orthophosphate is released from natural substrates, is unknown. However, we advocate that this process is important and that the rate of substrate supply, rather than phosphatase activity, limits the enzymatic phosphate regeneration.

Key words

phosphatases phosphate ester phosphorus deficiency phosphate regeneration lake water 

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References

  1. Aaronson, S., 1971. The synthesis of extracellular macromolecules and membranes by a population of the phytoflagellate Ochromonas Danica. Limnol. Oceanogr. 16: 1–9.Google Scholar
  2. Aaronson, S. & N. J. Patni, 1976. The role of surface and extracellular phosphatases in the phosphorus requirement of Ochromonas. Limnol. Oceanogr. 21: 838–845.Google Scholar
  3. Antia, N. J. & A. Watt, 1965. Phosphatase activity in some species of marine phytoplankters. J. Fish Res. Bd Can. 22: 793–799.Google Scholar
  4. Berman, T., 1969. Phosphatase release of inorganic phosphorus in Lake Kinneret. Nature 224: 1231–1232.Google Scholar
  5. Berman, T., 1970. Alkaline phosphatases and phosphorus availability in Lake Kinneret. Limnol. Oceanogr. 15: 663–674.Google Scholar
  6. Berman, T. & G. Moses, 1972. Phosphorus availability and alkaline phosphatase activities in two Israeli fishponds. Hydrobiologia 40: 487–498.Google Scholar
  7. Boavida, M. J. & R. T. Heath, 1984. Are the phosphatases released by Daphnia magna components of its food? Limnol. Oceanogr. 29: 641–645.Google Scholar
  8. Boavida, M. J., J. Spuij, D. Markowitz & R. T. Heath, 1984. Are soluble alkaline phosphatases secreted by zooplankton? Ohio J. Sci. 84: 77.Google Scholar
  9. Bothwell, M. L., 1985. Phosphorus limitation of lotic periphyton growth rates: An intersite comparison using continuous-flow troughs (Thompson River system, British Columbia). Limnol. Oceanogr. 30: 527–542.Google Scholar
  10. Brandes, D. & R. N. Elston, 1956. An electron microscopical study of the histochemical localization of alkaline phosphatase in the cell wall of Chlorella vulgaris. Nature 177: 274.Google Scholar
  11. Cembella, A. D., N. J. Antia & P. J. Harrison, 1984. The utilization of inorganic and organic phosphorus-compounds as nutrients by eukaryotic microalgae. — A multidisciplinary perspective. Part 1. CRC Crit. Rev. Microbiol. 10: 317–391.Google Scholar
  12. Chrost, R. J., W. Siuda & G. Halemejko, 1984. Longterm studies on alkaline phosphatase activity (APA) in a a lake with fish-aquaculture in relation to lake eutrophication and phosphorus cycle. Arch. Hydrobiol./Suppl. 70: 1–32.Google Scholar
  13. Corpe, W. A. & H. Winters, 1972. Hydrolytic enzymes of some periphytic marine bacteria. Can. J. Microbiol. 18: 1483–1490.Google Scholar
  14. Currie, D. J. & J. Kalff, 1984. A comparison of the abilities of freshwater algae and bacteria to acquire and retain phosphorus. Limnol. Oceanogr. 29: 298–310.Google Scholar
  15. Elgavish, A., M. Halmann & T. Berman, 1982. A comparative study of phosphorus utilization and storage in batch cultures of Peridinium cinctum, Pediastrum duplex and Cosmarium sp., from Lake Kinneret (Israel). Phycologia 21: 47–54.Google Scholar
  16. Feder, J., 1973. The phosphatases. In E. J. Griffith, A. Beeton, J. M. Spencer & D. T. Mitchell (eds), Environmental phosphorus handbook. J. Wiley & Sons. NY: 475–508.Google Scholar
  17. Fitzgerald, G. P. & T. C. Nelson, 1966. Extractive and enzymatic analyses for limiting or surplus phosphorus in algae. J. Phycol. 2: 32–37.Google Scholar
  18. Francko, D. A., 1983. Size-fractionation of alkaline phosphatase activity in lake water by membrane filtration. J. Fresh. Ecol. 2: 305–309.Google Scholar
  19. Francko, D. A., 1984a. Relationships between phosphorus functional classes and alkaline phosphatase activity in reservoir lakes. J. Fresh. Ecol. 2: 541–547.Google Scholar
  20. Francko, D. A., 1984b. Phytoplankton metabolism and cyclic nucleotides. II. Nucleotide-induced perturbations of alkaline phosphatase activity. Arch. Hydrobiol. 100: 409–421.Google Scholar
  21. Francko, D. A. & R. G. Wetzel, 1982. The isolation of cyclic adenosine 3′:5′-monophosphate (cAMP) from lakes of differing trophic status: Correlation with planktonic metabolic variables. Limnol. Oceanogr. 27: 27–38.Google Scholar
  22. Fuhs, G. W., S. D. Demmerle, E. Canelli & M. Chen, 1972. Characterization of phosphorus-limited plankton algae (with reflections on the limiting-nutrient concept). In G. E. Likens (ed.) Nutrients and eutrophication: The limiting-nutrient controversy. Am. Soc. Limnol. Oceanogr. Spec. Symp. 1: 113–133.Google Scholar
  23. Gage, M. A., 1978. Alkaline phosphatase activity in several Minnesota lakes. Doctoral thesis. University of Minnesota. 52 pp.Google Scholar
  24. Gage, M. A. & E. Gorham, 1985. Alkaline phosphatase activity and cellular phosphorus as an index of phosphorus status of phytoplankton in Minnesota lakes. Freshwat. Biol. 15: 227–223.Google Scholar
  25. Glew, R. H. & E. C. Heath, 1971. Studies on the extracellular alkaline phosphatase of Micrococcus sodonensis. I. Isolation and characterization. J. Biol. Chem. 246: 1556–1565.Google Scholar
  26. Gunatilaka, A., 1984. Observations on phosphorus dynamics and orthophosphate turnover in a tropical lake — Parakrama Samudra, Sri Lanka. Verh. int. Ver. Limnol. 22: 1567–1571.Google Scholar
  27. Halemejko, G. Z. & R. J. Chrost, 1984. The role of phosphatases in phosphorus mineralization during decomposition of lake phytoplankton blooms. Arch. Hydrobiol. 101: 489–502.Google Scholar
  28. Hassan, H. M. & D. Pratt, 1977. Biochemical and physiological properties of alkaline phosphatases EC-3.1.3.1 in isolates of marine bacteria. J. Bact. 129: 1607–1612.Google Scholar
  29. Healey, F. P., 1973. Characteristics of phosphorus deficiency in Anabaena. J. Phycol. 9: 383–394.Google Scholar
  30. Healey, F. P., 1985. Interacting effects of light and nutrient limitation on the growth rate of Synechococcus linearis (Cyanophyceae). J. Phycol. 21: 134–146.Google Scholar
  31. Healey, F. P. & L. L. Hendzel, 1979. Fluorometric measurement of alkaline phosphatase activity in algae. Freshwat. Biol. 9: 429–439.Google Scholar
  32. Healey, F. P. & L. L. Hendzel, 1980. Physiological indicators of nutrient deficiency in lake phytoplankton. Can. J. Fish. aquat. Sci. 37: 442–453.Google Scholar
  33. Heath, R. T. & G. D. Cooke, 1975. The significance of alkaline phosphatase in a eutrophic lake. Verh. int. Ver. Limnol. 19: 959–965.Google Scholar
  34. Huber, A. L. & K. S. Hamel, 1985. Phosphatase activities in relation to phosphorus nutrition in Nodularia spumigena (Cyanobacteriaceae). 1. Field studies. Hydrobiologia 123: 145–152.Google Scholar
  35. Huber, A. L. & D. K. Kidby, 1984a. An examination of the factors involved in determining phosphatase activities in estuarine water. 1: Analytical procedures. Hydrobiologia 111: 3–11.Google Scholar
  36. Huber, A. L. & D. K. Kidby, 1984b. An examination of the factors involved in determining phosphatase activities in estuarine waters. 2: Sampling procedures. Hydrobiologia 111: 13–19.Google Scholar
  37. Huber, A. L., J. O. Gabrielson, P. J. Dolin & D. K. Kidby, 1983. Decomposition of Cladophora. III. Heterotroph populations and phosphatase activity associated with in vitro phosphorus mineralization. Bot. mar. 26: 181–188.Google Scholar
  38. Ihlenfeldt, M. J. A. & J. Gibson, 1975. Phosphate utilization and alkaline phosphatase activity in Anacystis nidulans (Synechococcus). Arch. Microbiol. 102: 23–28.Google Scholar
  39. Jansson, M., 1975. Phosphatases in the Koukkel lakes. In Progress Report from the Kuokkel project 4: 119–131. Institute of Limnology, Uppsala, Sweden. (in swedish).Google Scholar
  40. Jansson, M., 1976. Phosphatases in lake water: Characterization of enzymes from phytoplankton and zooplankton by gel filtration. Science 194: 320–321.Google Scholar
  41. Jansson, M., 1977. Enzymatic release of phosphate in water from subarctic lakes in northern Sweden. Hydrobiologia 56: 175–180.Google Scholar
  42. Jansson, M., 1981. Induction of high phosphatase activity by aluminum in acid lakes. Arch. Hydrobiol. 93: 32–44.Google Scholar
  43. Jansson, M., H. Olsson & O. Broberg, 1981. Characterization of acid phosphatases in the acidified Lake Gårdsjön, Sweden. Arch. Hydrobiol. 92: 377–395.Google Scholar
  44. Jones, J. G., 1972a. Studies on freshwater bacteria: Association with algae and alkaline phosphatase activity. J. Ecol. 60: 59–75.Google Scholar
  45. Jones, J. G., 1972b. Studies on freshwater micro-organisms: phosphatase activity in lakes of differing degrees of eutrophication. J. Ecol. 60: 777–791.Google Scholar
  46. Klotz, R. L., 1985a. Influence of light on the alkaline phosphatase activity of Selenastrum capricornutum (Chlorophyceae) in streams. Can. J. Fish. aquat. Sci. 42: 384–388.Google Scholar
  47. Klotz, R. L., 1985b. Factors controlling phosphorus limitation in stream sediments. Limnol. Oceanogr. 30: 543–553.Google Scholar
  48. Kobori, H. & N. Taga, 1979a. Phosphatase activity and its role in the mineralization of organic phosphorus in coastal sea water. J. exp. mar. Biol. Ecol. 36: 23–39.Google Scholar
  49. Kobori, H. & N. Taga, 1979b. Occurrence and distribution of phosphatase in neritic and oceanic sediments. Deep Sea Res. 26A: 799–808.Google Scholar
  50. Kobori, H. & N. Taga, 1980. Extracellular alkaline phosphatase from marine bacteria: purification and properties of extracellular phosphatase from a marine Pseudomonas sp. Can. J. Microbiol. 26: 833–838.Google Scholar
  51. Kobori, H., N. Taga & U. Simudu, 1979. Properties and generic composition of phosphatase-producing bacteria in coastal and oceanic seawater. Bull. jap. Soc. Sci. Fish. 45: 1429–1433.Google Scholar
  52. Kuenzler, E. J., 1965. Glucose-6-phosphate utilization by marine algae. J. Phycol. 1: 156–164.Google Scholar
  53. Kuenzler, E. J. & J. P. Perras, 1965. Phosphatases of marine algae. Biol. Bull. Woods Hole. 128: 271–284.Google Scholar
  54. Lien, T. & G. Knutsen, 1973. Synchronous cultures of Chlamydomonas reinhardti: Properties and regulation of repressible phosphatases. Physiol. Pl. 28: 291–298.Google Scholar
  55. Lin, C. K., 1977. Accumulation of water soluble phosphorus and hydrolysis of polyphosphates by Cladophora glomerata (Chlorophyceae). J. Phycol. 13: 46–51.Google Scholar
  56. Livingstone, D. & B. A. Whitton, 1984. Water chemistry and phosphatase activity of the blue-green algae Rivularia in Upper Teesdale streams. J. Ecol. 72: 405–421.Google Scholar
  57. Livingstone, D., T. M. Khoja & B. A. Whitton, 1983. Influence of phosphorus on physiology of a hair-forming blue-green algae (Calotrix parietina) from an upland stream. Phycologia 22: 345–350.Google Scholar
  58. Matavulj, M., S. Gajin, M. Gantar, O. Petrovic, M. Erbeznik, M. Bokorov & S. Stojilkovic, 1984. Phosphatase activity as an additional parameter of water condition estimate in some lakes of Vojvodina province. Mikrobiologija 21: 53–62.Google Scholar
  59. McComb, R. B., G. N. Bowers & S. Posen, 1979. Alkaline phosphatases. Plenum Press, NY, 986 pp.Google Scholar
  60. Møller, M., S. Myklestad & A. Haug, 1975. Alkaline and acid phosphatases of the marine diatoms Chaetoceras affinis var. Willei (Gran) Hustedt and Skeletonema costatum (Grev.) Cleve. J. exp. mar. Biol. Ecol. 19: 217–226.Google Scholar
  61. Oláh, J. & E. O. Toth, 1978. The function of alkaline phosphatase enzyme in the phosphorus cycle of fertilized fishponds. Aquacultura Hungarica 1: 15–23.Google Scholar
  62. Olsen, Y., G. Knutsen & T. Lien, 1983. Characteristics of phosphorus limitation in Chlamydomonas reinhardtii (Chlorophyceae) and its palmelloids. J. Phycol. 19: 313–319.Google Scholar
  63. Olsson, H., 1983. Origin and production of phosphatases in the acid Lake Gårdsjön. Hydrobiologia 101: 49–58.Google Scholar
  64. Overbeck, J., 1962. Untersuchungen zum Phosphathaushalt von Grünalgen. II. Die Verwertung von Pyrophosphat und organisch gebundenen Phosphaten und ihre Beziehung zu den Phosphatasen von Schenedesmus quadricauda (Turp.) Bré. Arch. Hydrobiol. 58: 281–308.Google Scholar
  65. Overbeck, J. & H.-D. Babenzien, 1964. Uber den Nachweis von freien Enzymen im Gewässer. Arch. Hydrobiol. 60: 107–114.Google Scholar
  66. Patni, N. J., S. W. Dawale & S. Aaronson, 1977. Extracellular phosphatases of Chlamydomonas reinhardi and their regulation. J. Bact. 130: 205–211.Google Scholar
  67. Perry, M. J., 1972. Alkaline phosphatase activity in subtropical Central North Pacific waters using a sensitive fluorometric method. Mar. Biol. 15: 113–119.Google Scholar
  68. Pettersson, K., 1985. Alkaline phosphatase activity and algal surplus phosphorus as phosphorus-deficiency indicators in Lake Erken. Arch. Hydrobiol. 89: 54–87.Google Scholar
  69. Pettersson, K., 1985. The availability of phosphorus and the species composition of the spring phytoplankton in Lake Erken. Int. Revue ges. Hydrobiol. 70: 527–546.Google Scholar
  70. Pettersson, K. & M. Jansson, 1978. Determination of phosphatase activity in lake water — a study of methods. Verh. int. Ver. Limnol. 20: 1226–1230.Google Scholar
  71. Price, C. A., 1962. Repression of acid phosphatase synthesis in Euglena gracilis. Science 135: 46.Google Scholar
  72. Reichardt, W., 1971. Catalytic mobilization of phosphate in lake water and by Cyanophyta. Hydrobiologia 38: 377–394.Google Scholar
  73. Reichardt, W., 1973. Das Reaktionspotential in Ökosystemen Zur Problematik limnologischer Enzymanalysen. Arch. Hydrobiol./Suppl. 42: 253–272.Google Scholar
  74. Reichardt, W., 1978. Responses of phosphorus remobilizing cytophaga species to nutritional and thermal stress. Verh. int. Ver. Limnol. 20: 2227–2232.Google Scholar
  75. Reichardt, W. & J. Overbeck, 1969. Zur enzymatischen Regulation der Phosphatmonoesterhydrolyse durch Cyanophyceenplankton. Ber. dtsch. Bot. Ges. 81: 391–396.Google Scholar
  76. Reichardt, W., J. Overbeck & L. Steubing, 1967. Free dissolved enzymes in lake waters. Nature 216: 1345–1347.Google Scholar
  77. Rigler, F. H., 1961. The uptake and release of inorganic phosphorus by Daphnia magna Straus. Limnol. Oceanogr. 6: 165–174.Google Scholar
  78. Rivkin, R. B. & E. Swift, 1979. Diel and vertical patterns of alkaline phosphatase activity in the oceanic dinoflagellate Pyrocystis nocticula. Limnol. Oceanogr. 24: 107–116.Google Scholar
  79. Rivkin, R. B. & E. Swift, 1980. Characterization of alkaline phosphatase and organic phosphorus utilization in the oceanic dinoflagellate Pyrocystis nocticula. Mar. Bot. 61: 1–8.Google Scholar
  80. Schmitter, R. E. & A. J. Jurkiewicz, 1981. Acid phosphatase localization in peri iodic-acid schiff bodies of Gonyaulax. J. Cell Sci. 51: 15–24.Google Scholar
  81. Siuda, W., 1984. Phosphatases and their role in organic phosphorus transformation in natural waters. A review. Pol. Arch. Hydrobiol. 31: 207–233.Google Scholar
  82. Smith, R. E. H. & J. Kalff, 1981. The effect of phosphorus limitation of algal growth rates: evidence from alkaline phosphatase. Can. J. Fish. aquat. Sci. 38: 1421–1427.Google Scholar
  83. Spiro, T. G., 1973. Phosphate transfer and its activation by metal ions; alkaline phosphatase. In G. L. Eichhorn (ed.), Inorganic Biochemistry. Vol. 1. Elsevier Sci. Publ. Co., Amsterdam: 549–581.Google Scholar
  84. Sproule, J. L. & J. Kalff, 1978. Seasonal cycles in the phytoplankton phosphorus status of a north temperate zone lake (Lake Memphremagog, Que-Vt), plus a comparison of techniques. Verh. int. Ver. Limnol. 20: 2681–2688.Google Scholar
  85. Steiner, M., 1938. Zur Kenntnis der Phosphatkreislaufes in Seen. Naturwissenschaften 26: 723–724.Google Scholar
  86. Stewart, A. J. & R. G. Wetzel, 1982a. Phytoplankton contribution to alkaline phosphatase activity. Arch. Hydrobiol. 93: 265–271.Google Scholar
  87. Stewart, A. J. & R. G. Wetzel, 1982b. Influence of dissolved humic materials on carbon assimilation and alkaline phosphatase activity in natural algal-bacterial assemblages. Freshwat. Biol. 12: 369–380.Google Scholar
  88. Stevens, R. J. & M. P. Parr, 1977. The significance of alkaline phosphatase activity in Lough Neagh. Freshwat. Biol. 7: 351–355.Google Scholar
  89. Taft, J. L., M. E. Loftus & W. R. Taylor, 1977. Phosphate uptake form phosphomonoesters by phytoplankton in the Chesapeake Bay. Limnol. Oceanogr. 22: 1012–1021.Google Scholar
  90. Talpasayi, E. R. S., 1962. Acid phosphatase activity of some algae and its inhibition by molybdenum. Biochim. Biophys. Acta 59: 710–712.Google Scholar
  91. Thompson, L. M. M. & R. A. MacLeod, 1974a. Factors affecting the activity and stability of alkaline phosphatase in a marine pseudomonad. J. Bact. 117: 813–818.Google Scholar
  92. Thompson, L. M. M. & R. A. MacLeod, 1974b. Biochemical localization of alkaline phosphatase in the cell wall of a marine pseudomonad. J. Bact. 117: 819–825.Google Scholar
  93. Tiwari, B. K. & R. R. Mishra, 1982. A study on biological activity measurements and heterotrophic bacteria in a small freshwater lake. Hydrobiologia 94: 257–267.Google Scholar
  94. Verstraete, W., J. P. Voets & P. vanLancker, 1976. Evaluation of some enzymatic methods to measure the bioactivity of aquatic environments. Hydrobiologia 49: 257–266.Google Scholar
  95. Vincent, W. F., 1981. Rapid physiological assays for nutrient demand by the plankton. II. Phosphorus. J. Plankton Res. 3: 699–710.Google Scholar
  96. Walther, K. & L. Fries, 1976. Extracellular alkaline phosphatase in multicellular marine algae and their utilization of glycerophosphate. Physiol. Pl. 36: 118–122.Google Scholar
  97. Wetzel, R. G., 1981. Longterm dissolved and particulate alkaline phosphatase activity in a hardwater lake in relation to lake stability and phosphorus enrichments. Ver. int. Ver. Limnol. 21: 369–381.Google Scholar
  98. Wilkins, A. S., 1972. Physiological factors in the regulation of alkaline phosphatase synthesis in Escherichia coli. J. Bact. 110: 616–623.Google Scholar
  99. Wynne, D., 1977. Alternations in activity of phosphatases during the Peridinium bloom in Lake Kinneret. Physiol. Pl. 40: 219–224.Google Scholar
  100. Wynne, D., 1981. The role of phosphatases in the metabolism of Peridinium cinctum, from Lake Kinneret. Hydrobiologia 83: 93–99.Google Scholar
  101. Wynne, D. & M. Gophen, 1981. Phosphatase activity in freshwater zooplankton. Oikos 37: 369–376.Google Scholar
  102. Yentsch, C. M., C. S. Yentsch & J. P. Parras, 1972. Alkaline phosphatase activity in the tropical marine blue-green alga, Oscillatoria erythraea (‘Trichodesmium’). Limnol. Oceanogr. 17: 772–774.Google Scholar

Copyright information

© Kluwer Academic Publishers 1988

Authors and Affiliations

  • Mats Jansson
    • 1
  • Håkan Olsson
    • 1
  • Kurt Pettersson
    • 1
  1. 1.Institute of LimnologyUppsalaSweden

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