Skip to main content
SpringerLink
Log in

Phosphatase activity of benthic marine algae. An overview

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

This review provides an account of the phosphatase activities of benthicmarine algae and is based on reports for more than a hundred species, includingcyanobacteria, red, brown and green algae. Particular emphasis is given to theuse of phosphomonoesterase activity as a rapid means of assessing thephosphorusstatus of the alga and thus indirectly that of the environment. Anunderstandingof the influence of environmental factors and the growth pattern of theparticular alga is important in carrying out assays. For instance, the responseto light differs markedly between species, especially in short-term assays,whenthe effect can be obvious or none. Considerations about the methodology formeasuring "alkaline phosphatase activity" are discussed, particularly whethertosimulate field conditions or to use optimum conditions. Recommendations aresuggested concerning the best methodology for routine use, followed by adiscussion of the future prospects for the method.

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

Similar content being viewed by others

References

  • Atkinson M.J. and Smith S.V. 1983. C:N:P ratios of benthic marine plants. Limnol. Oceanogr. 28: 568-574.

    Google Scholar 

  • Benitez-Nelson C.R. and Buesseler K.O. 1998. Variability of inorganic and organic phosphorus turnover rates in the coastal ocean. Nature 398: 502-505.

    Google Scholar 

  • Bentzen E., Taylor W.D. and Millard E.S. 1992. The importance of dissolved organic phosphorus to phosphorus uptake by limnetic plankton. Limnol. Oceanogr. 37: 217-231.

    Google Scholar 

  • Boavida M.J. and Heath R.T. 1986. Phosphatase activity of Chlamydomonas acidophila Negoro (Volvocales, Chlorophyceae). Phycologia 25: 400-404.

    Google Scholar 

  • Burkholder J.M. and Wetzel R.G. 1990. Epiphytic alkaline phosphatase on natural and artificial plants in an oligotrophic lake: re-evaluation of the role of macrophytes as a phosphorus source for epiphytes. Limnol. Oceanogr. 35: 736-747.

    Google Scholar 

  • Camarero L. 1994. Assay of soluble reactive phoshorus at nanomolar levels in nonsaline waters. Limnol. Oceanogr. 39: 707-711.

    Google Scholar 

  • Cembella A.D., Antia N.J. and Harrison P.J. 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 

  • Davies A.G. and Smith M.A. 1988. Alkaline phosphatase activity in the western English Channel. J. Mr. Biol. Ass. U.K. 68: 239-250.

    Google Scholar 

  • Delgado O. and Lapointe B.E. 1994. Nutrient-limited productivity of calcareous versus fleshy macroalgae in a eutrophic, carbonate-rich tropical marine environment. Coral Reefs 13: 151-159.

    Google Scholar 

  • Delgado O., Rodríguez-Prieto C., Gacia E. and Ballesteros E. 1996. Lack of severe nutrient limitation in Caulerpa taxifolia (Vahl) C. Agardh, an introduced seaweed spreading over the oligotrophic Northwestern Mediterranean. Bot. mar. 39: 61-67.

    Google Scholar 

  • Dixon M. and Webb E.C. 1979. Enzymes. 3rd edn. Longman, London.

    Google Scholar 

  • Duarte C.M. 1992. Nutrient concentration of aquatic plants: patterns across species. Limnol. Oceanogr. 37: 882-889.

    Google Scholar 

  • Durrieu C. and Tran-Minh C. 2002. Optical algal bioisesndor using alkaline phosphatase for determination of heavy metals. Ecotoxicol. Environ. Saf. 51: 206-209.

    Google Scholar 

  • Dyhrman S.T. and Palenik B.P. 1997. The identification and puri-fication of a cell-surface alkaline phosphatase from the dinoflagellate Prorocentrum minimum (Dinophyceae). J. Phycol. 33: 602-612.

    Google Scholar 

  • Dyhrman S.T. and Palenik B.P. 1999. Phosphate stress in cuntures and field populations of the dinoflagellate Prorocentrum minimum detected using a single-cell alkaline phosphatase activity assay. Appl. environ. Microbiol. 65: 3205-3212.

    Google Scholar 

  • Dyhrman S.T. and Palenik B. 2001. A single-cell immunoassay for phosphate stress in the dinoflagellate Prorocentrum minimum (Dinophyceae). J. Phycol. 37: 400-410.

    Google Scholar 

  • Falkowski G.P. and Raven J.A. 1997. Aquatic Photosynthesis. Blackwell, Malden, Massachusetts, USA.

    Google Scholar 

  • Fedde K.N. and Whyte M.P. 1990. Alkaline phosphatase (tissuenonspecific isoenzyme) is a phosphoethanolamine and pyridoxal-5′-phosphate ectophosphate: normal and hypophosphatasia fibroblast study. Am. J. Hum. Genet. 47: 767-775.

    Google Scholar 

  • Fitzgerald G.P. and Nelson C. 1966. Extractive and enzymatic analyses for limiting or surplus phosphorus in algae. J. Phycol. 2:32-37.

    Google Scholar 

  • Flores-Moya A., Altamirano M., Cordero M., González M.E. and Pérez M.G. 1997. Phosphorus-limited growth in the seasonal winter red alga Porphyra leucosticta Thuret in le Jolis. Bot. mar. 40: 187-191.

    Google Scholar 

  • Flynn K.J., Opik H. and Syrett P.J. 1986. Localization of alkalinephosphatase and 5′-nucleotidase activities of the diatom Phaeodactylum tricornutum. J. gen. Microbiol. 132: 289-298.

    Google Scholar 

  • Fogg G.E. 1973. Phosphorus in primary aquatic plants. Wat. Res. 7: 77-91.

    Google Scholar 

  • Francko D.A. and Heath R.T. 1979. Functionally distint classes of complex phosphorus compounds in lake water. Limnol. Oceanogr. 24: 463-473.

    Google Scholar 

  • Gantt E. 1990. Pigmentation and photoacclimation. In: Cole K.M. and Sheath R.G. (eds), Biology of the Red Algae. Cambridge University Press, Cambridge, pp. 203-219.

    Google Scholar 

  • García-Ruiz R., Hernández I., Lucena J. and Niell F.X. 1997. Preliminary studies on the significance of alkaline phosphatase activity in the diatom Phaeodactylum tricornutum Bohlin. Sci. Mar. 61: 517-525.

    Google Scholar 

  • González-Gil S., Keafer B.A., Jovine R.V.M., Aguilera A., Lu S. and Anderson D.M. 1998. Detection and quantification of alkaline phosphatase in single cells of phosphorus-starved marine phytoplankton. Mar. Ecol. Progr. Ser. 164: 21-35.

    Google Scholar 

  • Grainger S.L.J., Peat A., Tiwari D.N. and Whitton B.A. 1989. Phosphomonoesterase activity of the cyanobacterium (blue-green alga) Calothrix parietina. Microbios 59: 1-17.

    Google Scholar 

  • Hantke B. and Melzer A. 1993. Kinetic changes in surface phosphatase activity of Synedra acus (Bacillariophyceae) in relation to pH variation. Freshwat. Biol. 29: 31-36.

    Google Scholar 

  • Heath R.T. 1986. Dissolved organic compounds: do they satisfy planktonic phosphate demand in summer? Can. J. Fish. Aquat. Sci. 43: 343-350.

    Google Scholar 

  • Hein M., Pedersen M.F. and Sand-Jensen K. 1995. Size-dependent nitrogen uptake in micro-and macroalgae. Mar. Ecol. Progr. Ser. 118: 247-253.

    Google Scholar 

  • Henley W.J. 1993. Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J. Phycol. 29: 729-739.

    Google Scholar 

  • Hernández I. 1996. Analysis of the expression of alkaline phosphatase activity as a measure of phosphorus status in the red alga Porphyra umbilicalis (L.) Kützing. Bot. Mar. 39: 255-262.

    Google Scholar 

  • Hernández I., Andría J.R., Christmas M. and Whitton B.A. 1999. Testing the allometric scaling of alkaline phosphatase activity to surface/volume ratio in benthic marine macrophytes. J. Exp.Mar. Biol. Ecol. 241: 1-14.

    Google Scholar 

  • Hernández I., Christmas M., Yelloly J. and Whitton B.A. 1997. Factors affecting surface alkaline phosphatase activity in the brown alga Fucus spiralis at a North Sea intertidal site (Tyne Sands, Scotland). J. Phycol. 33: 569-575.

    Google Scholar 

  • Hernández I., Fernández J.A. and Niell F.X. 1993. Influence of phosphorus status on the seasonal variation of alkaline phosphatase activity in Porphyra umbilicalis (L.) Kützing. J. Exp.Mar. Biol. Ecol. 173: 181-196.

    Google Scholar 

  • Hernández I., Fernández J.A. and Niell F.X. 1995. A comparative study of alkaline phosphatase activity of two species of Gelidium (Gelidiales, Rhodophyta). Eur. J. Phycol. 30: 69-77.

    Google Scholar 

  • Hernández I., Hwang S.-J. and Heath R.T. 1996b. Measurement of phosphomonoesterase activity with a radiolabelled glucose-6-phosphate. Role in the phosphorus requirement of phytoplankton and bacterioplankton in a temperate mesotrophic lake. Arch. Hydrobiol. 137: 265-280.

    Google Scholar 

  • Hernández I., Niell F.X. and Fernández J.A. 1992. Alkaline phosphatase activity in Porphyra umbilicalis (L.) Kützing. J. Exp. Mar. Biol. Ecol. 159: 1-13.

    Google Scholar 

  • Hernández I., Niell F.X. and Fernández J.A. 1994b. Alkaline phosphatase activity in marine macrophytes. Study of its localization in some widespread species in southern Spain. Mar. Biol. 120: 501-509.

    Google Scholar 

  • Hernández I., Niell F.X. and Fernández J.A. 1996a. Alkaline phosphatase activity of the red alga Corallina elongata Ellis et Solander. Sci. Mar. 60: 297-306.

    Google Scholar 

  • Hernández I., Pérez-Lloréns J.L., Fernández J.A. and Niell F.X. 1994a. Alkaline phosphatase activity in Zostera noltii Hornem. and its contribution to the release of phosphate in the Palmones river estuary. Est. Coast. Shelf Sci. 39: 461-476.

    Google Scholar 

  • Hernández I., Pérez-Pastor A. and Pérez-Lloréns J.L. 2000. Ecological significance of phosphomonoesters and phosphomonoesterase activity in a small Mediterranean river and its estuary. Aquat. Ecol. 34: 107-117.

    Google Scholar 

  • Hernández I. and Whitton B.A. 1996. Retention of p-nitrophenol and 4-methylumbelliferone by marine macroalgae and implications for measurement of alkaline phosphatase activity. J. Phycol. 32: 819-825.

    Google Scholar 

  • Hines M.E. and Lyons W.B. 1982. Biogeochemistry of nearshore Bermuda sediments. I. Sulfate reduction rates and nutrient regeneration. Mar. Ecol. Progr. Ser. 8: 87-95.

    Google Scholar 

  • Hoppe H.-G. Phosphatase activity in the sea. Hydrobiologia (in press).

  • Huang B. and Hong H. 1999. Alkaline phosphatase activity and utilization of dissolved organic phosphorus by algae in subtropical coastal waters. Mar. Pol. Bull. 39: 205-211.

    Google Scholar 

  • Hurd C.L. and Dring M.J. 1990. Phosphate uptake by intertidal algae in relation to zonation and season. Mar. Biol. 107: 281-289.

    Google Scholar 

  • Invers O., Pérez M. and Romero J. 1995. Alkaline phosphatase activity as tool for assessing nutritional conditions in the seagrass Posidonia oceanica (L.) Delile. Sci. Mar. 59: 41-47.

    Google Scholar 

  • Jansson M., Olsson H. and Pettersson K. 1988. Phosphatase; origin, characteristics and function in lakes. Hydrobiologia 170: 157-175.

    Google Scholar 

  • Karl D.M. and Yanagi K. 1997. Partial characterization of the dissolved organic phosphorus pool in the oligotrophic North Pacific Ocean. Limnol. Oceanogr. 42: 1398-1405.

    Google Scholar 

  • Klotz R.L. 1985. Influence of light on the alkaline phosphatase activity of Selenastrum capricornutum (Chlorophyceae) in streams. Can. J. Fish. Aquat. Sci. 42: 384-388.

    Google Scholar 

  • Kobori H. and Taga N. 1979. 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 

  • Kolowith L.C., Ingall E.D. and Benner R. 2001. Composition and cycling of marine organic phosphorus. Limnol. Oceanogr. 46: 309-330.

    Google Scholar 

  • Kuenzler E.J. 1965. Glucose-6-phosphate utilization by marine algae. J. Phycol. 1: 156-164.

    Google Scholar 

  • Küppers U. and Weidner U. 1980. Seasonal variation of enzyme activities in Laminaria hyperborea. Planta 148: 222-230.

    Google Scholar 

  • Lapointe B.E. 1989. Macroalgal production and nutrient relations in oligotrophic areas of Florida Bay. Bull. Mar. Sci. 44: 312-323.

    Google Scholar 

  • Lapointe B.E. 1997. Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and Southeast Florida. Limnol. Oceanogr. 45: 1119-1131.

    Google Scholar 

  • Lapointe B.E., Littler M.M. and Littler D.S. 1992. Nutrient availability to marine macroalgae in siliciclastic versus carbonaterich coastal waters. Estuaries 15: 75-82.

    Google Scholar 

  • Lapointe B.E., Tomasko D.A. and Matzie W.R. 1994. Eutrophication and trophic state classification of seagrass communities in the Florida Keys. Bull. Mar. Sci. 54: 696-717.

    Google Scholar 

  • Larsson C., Axelsson L., Ryberg H. and Beer S. 1997. Photosynthetic carbon utilization by Enteromorpha intestinalis (Chlorophyta) from a Swedish rockpool. Eur. J. Phycol. 32: 49-54.

    Google Scholar 

  • Lee T.M. 2000. Phosphate starvation induction of acid phosphatase in Ulva lactuca L. (Ulvales, Chlorophyta). Bot. Bull. Acad. Sin. 41: 19-25.

    Google Scholar 

  • Lee T.M., Tsai C.C. and Shih M.C. 1999. Induction of phosphorus deficiency and phosphatase activity by salinity (NaCl) stress in Gracilaria tenuistipitata (Gigartinales, Rhodophyta). Phycologia 38: 428-433.

    Google Scholar 

  • Levitzki A. and Koshland D.E.Jr 1976. The role of negative cooperativity and half-of-the-sites reactivity in enzyme regulation. In: Horecker B.L. and Stadtman E.R. (eds), Current Topics in Cell Regulation. Vol. 10. Academic Press, New York, pp.1-40.

    Google Scholar 

  • Littler M.M., Littler D.S. and Titlyanov E.A. 1991. Comparisons of N-and P-limited productivity between high granitic islands versus low carbonate atolls in the Seychelles Archipelago: a test of the relative-dominance paradigm. Coral Reefs 10: 199-209.

    Google Scholar 

  • Mahasneh I.A., Grainger S.L.J. and Whitton B.A. 1990. Influence of salinity on hair formation and phosphatase activities of the blue-green alga (cyanobacterium) Calothrix viguieri D253. Br. phycol. J. 25: 25-32.

    Google Scholar 

  • Mann N.H. 2000. Detecting the environment. In: Whitton B.A. and Potts M. (eds), Ecology of Cyanobacteria. Kluwer Academic Publishers, Dordrecht, pp. 367-395.

    Google Scholar 

  • McComb R.B., Bowers G.N. and Posen S. 1979. Alkaline Phosphatase. Plenum Press, New York.

    Google Scholar 

  • Murphy J. and Riley J.P. 1962. A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta. 27: 31-36.

    Google Scholar 

  • Nielsen S.L., Enríquez S., Duarte C.M. and Sand-Jensen K. 1996. Scaling maximum growth rates across photosynthetic organisms. Functional Ecol. 10: 167-175.

    Google Scholar 

  • Nixon S.W., Kelly J.R., Furnas B.N., Oviatt C.A. and Hale S.S. 1980. Phosphorus regeneration and the metabolism of coastal marine bottom communities. In: Tenore K.R. and Coull B.C. (eds), Marine Benthic Dynamics. University of South Carolina Press, Columbia, South Carolina, USA, pp. 219-242.

    Google Scholar 

  • Pérez M. and Romero J. 1993. Preliminary data on alkaline phosphatase activity associated with Mediterranean seagrasses. Bot. mar. 26: 499-502.

    Google Scholar 

  • Perry M.J. 1972. Alkaline phosphatase activity in subtropical Central North Pacific waters. Mar. Biol. 15: 113-119.

    Google Scholar 

  • Pettersson K. and Jansson M. 1978. Determination of phosphatase activity in lake water. A study of methods. Verh. int. Verein. Limnol. 20: 1226-1230.

    Google Scholar 

  • Pick F.R. 1987. Interpretations of alkaline phosphatase activity in Lake Ontario. Can. J. Fish. aquat. Sci. 44: 2087-2094.

    Google Scholar 

  • Price N.C. and Stevens L. 1982. Fundamentals of Enzymology. Oxford University Press, Oxford.

    Google Scholar 

  • Rivkin R.B. and Swift E. 1980. Characterization of alkaline phosphatase and organic phosphorus utilization in the oceanic dinoflagellate Pyrocystis noctiluca. Mar. Biol. 61: 1-8.

    Google Scholar 

  • Scanlan D.J. and Wilson W.H. 1999. Application of molecular techniques to addressing the role of P as a key effector in marine ecosystems. Hydrobiologia 401: 149-175.

    Google Scholar 

  • Schaffelke B. 2001. Surface alkaline phosphatase activities of macroalgae on coral reefs of the central Great barrier Reef, Australia. Coral Reefs 19: 310-317.

    Google Scholar 

  • Shan Y., McKelvie I.D. and Hart B.T. 1994. Determination of alkaline phosphatase-hydrolyzable phosphorus in natural water systems by enzymatic flow injection. Limnol. Oceanogr. 39: 1993-2000.

    Google Scholar 

  • Siuda W. 1984. Phosphatases and their role in organic phosphorus transformations in natural waters. A review. Pol. Arch. Hydrobiol. 31: 207-233.

    Google Scholar 

  • Stewart A.J. and Wetzel R.G. 1982. Influence of dissolved humic materials on carbon assimilation and alkaline phosphatase activity in natural algal-bacterial assemblages. Freshwat. Biol. 12: 369-380.

    Google Scholar 

  • Suzumura M., Ishikawa K. and Ogawa H. 1998. Characterization of dissolved organic phosphorus in coastal seawater using ultrafiltration and phosphohydrolytic enzymes. Limnol. Oceanogr. 43: 1553-1564.

    Google Scholar 

  • Thingstad T.F. and Rassoulzadegan F. 1995. Nutrient limitations, microbial food webs, and “;biological C-pumps”;: suggested interactions in a P-limited Mediterranean. Mar. Ecol. Progr. Ser. 117: 99-306.

    Google Scholar 

  • Thompson S.M. and Valiela I. 1999. Effect of nitrogen loading on enzyme activity in estuarioes in Waquoit bay. Bot. Mar. 42: 519-529.

    Google Scholar 

  • Touchette B.W. and Burkholder J.M. 2000. Review of nitrogen and phosphorus metabolism in seagrasses. J. Exp. Mar. Biol. Ecol. 250: 133-167.

    Google Scholar 

  • Turner B.L. and Haygarth P.M. 1999. Phosphorus leaching under cut grassland. Wat. Sci. Technol. 39: 63-67.

    Google Scholar 

  • Walter K. and Fries L. 1976. Extracellular alkaline phosphatase in multicellular marine algae and their utilization of glicerophosphate. Physiol. Plant 36: 118-122.

    Google Scholar 

  • Weich R.G. and Granéli E. 1989. Extracellular alkaline phosphatase activity in Ulva lactuca L. J. exp. Mar. Biol. Ecol. 129: 33-44.

    Google Scholar 

  • Whitton B.A., Grainger S.L.J., Hawley G.R.W. and Simon J.W. 1991. Cell bound and extracellular phosphatase activities of cyanobacterial isolates. Microb. Ecol. 21: 85-98.

    Google Scholar 

  • Whitton B.A., Potts M., Simon J.W. and Grainger S.L.J. 1990. Phosphatase activity of the blue-green alga (cyanobacterium) Nostoc commune UTEX 548. Phycologia 29: 139-145.

    Google Scholar 

  • Whitton B.A., Yelloly J.M., Christmas M. and Hernández I. 1998. Surface phosphatase activity of benthic algae in a stream with highly variable ambient phosphate concentration. Verh. int. Verein. Limnol. 26: 967-972.

    Google Scholar 

  • Wynne D. and Rhee G.Y. 1988. Changes in alkaline phosphatase activity and phosphate uptake in P-limited phytoplankton, induced by light intensity and spectral quality. Hydrobiologia 160: 173-178.

    Google Scholar 

  • Yelloly J.M. and Whitton B.A. 1996. Seasonal changes in ambient phosphate and phosphatase activities of the cyanobacterium Rivularia atra in intertidal pools at Tyne Sands, Scotland. Hydrobiologia 325: 201-212.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Área de Ecología, Facultad de Ciencias del Mar y Ambientales, Universidad de Cádiz, Puerto Real, 11510, Spain

    Ignacio Hernández

  2. Departamento de Ecología, Facultad de Ciencias Biológicas, Universidad de Málaga, Málaga, Spain

    F. Xavier Niell

  3. School of Biological and Biomedical Sciences, University of Durham, Durham, DH1 3LE, UK

    Brian A. Whitton

Authors
  1. Ignacio Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Xavier Niell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brian A. Whitton
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hernández, I., Niell, F.X. & Whitton, B.A. Phosphatase activity of benthic marine algae. An overview. Journal of Applied Phycology 14, 475–487 (2002). https://doi.org/10.1023/A:1022370526665

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022370526665

Search

Navigation