Skip to main content
SpringerLink
Log in

Silicon Deficiency Induces Alkaline Phosphatase Enzyme Activity in Cultures of Four Marine Diatoms

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

Alkaline phosphatase (AP) was detected using ELF-97® in silicon-starved Pseudo-nitzschia multiseries cells; thus, we tested two, alternative hypotheses: Pseudo-nitzschia multiseries has a high phosphate demand, showing signs of phosphate deficiency even when concentrations of orthophosphate are high, or silicate deficiency can stimulate the AP enzyme in this species. We also studied the effect of silicon deficiency on AP in three other common marine diatoms: Thalassiosira pseudonana, Nitzschia pusilla, and Nitschia closterium. Each of the species tested showed a different pattern of AP regulation. AP levels, however, increased in the four diatoms as a result of silicon deficiency, suggesting that AP may be involved in a variety of intracellular processes related to silicon deficiency. Additionally, the results of this study indicate that AP could be stimulated by stressors other than phosphate deficiency, such as silicon deficiency; therefore, it should be used cautiously as an indicator of phosphate limitation.

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

Similar content being viewed by others

Notes

  1. Use of trade names does not imply endorsement by NOAA Fisheries Service.

References

  • Berges, J.A., and P.G. Falkowski. 1998. Physiological stress and cell death in marine phytoplankton: induction of proteases in response to nitrogen or light limitation. Limnol Oceanogr 43: 129–135.

    Article  CAS  Google Scholar 

  • Bidle, K.D., and S.J. Bender. 2008. Iron starvation and culture age activate metacaspases and programmed cell death in the marine diatom Thalassiosira pseudonana. Eukaryotic Cell 7: 223–236.

    Article  CAS  Google Scholar 

  • Butow, B., D. Wynne, A. Sukenik, O. Hadas, and E. Tel-Or. 1998. The synergistic effect of carbon concentration and high temperature on lipid peroxidation in Peridinium gatunense. J Plankton Res 20: 355–369.

    Article  CAS  Google Scholar 

  • Cembella, A.D., N.J. Antia, and P.J. Harrison. 1984. The utilization of inorganic and organic phosphorus compounds as nutrients by eukaryotic microalgae: a multidisciplinary perspective: part 1. Crit Rev Microbiol 10: 317–91.

    Article  CAS  Google Scholar 

  • Chisholm, S.W., F. Azam, and R.W. Eppley. 1978. Silicic acid incorporation in marine diatoms on light:dark cycles: use of an assay for phased cell division. Limnol Oceanogr 23: 518–529.

    Article  CAS  Google Scholar 

  • Coleman, J.E. 1992. Structure and mechanism of alkaline phosphatase. Annu Rev Biophys Biomol Struct 21: 441–483.

    Google Scholar 

  • Coombs, J., P.J. Halicki, O. Holm-Hansen, and B.E. Volcani. 1967. Studies on the biochemistry and fine structure of silica shell formation in diatoms: changes in concentration of nucleoside triphosphates during synchronized division of Cylindrotheca fusiformis Reimann and Lewin. Exp. Cell Res 47: 302–314.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dyhrman, S.T., and K.C. Ruttenberg. 2006. Presence and regulation of alkaline phosphatase activity in eukaryotic phytoplankton from the coastal ocean: Implications for dissolved organic phosphorus remineralization. Limnol Oceanogr 51: 1381–1390.

    Article  CAS  Google Scholar 

  • Fleury, C., B. Mignotte, and J.L. Vayssiere. 2002. Mitochondrial reactive oxygen species in cell death signaling. Biochimie 84: 131–141.

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Gillard, J., V. Devos, M.J.J. Huysman, L. De Veylder, S. D'Hondt, C. Martens, P. Vanormelingen, K. Vannerum, K. Sabbe, V.A. Chepurnov, D. Inzé, M. Vuylsteke, and W. Vyverman. 2008. Physiological and transcriptomic evidence for a close coupling between chloroplast ontogeny and cell cycle progression in the pennate diatom Seminavis robusta. Plant Physiol 148: 1394–1411.

    Article  CAS  Google Scholar 

  • Hansen, H.P., and F. Koroleff. 1999. Determination of nutrient. In Methods of seawater analysis, ed. K. Grasshoff, K. Kremling, and M. Ehrhardt, 159–228. Weinheim: Wiley.

    Chapter  Google Scholar 

  • Harpole, W.S., J.T. Ngai, E.E. Cleland, E.W. Seabloom, E.T. Borer, M.E.S. Bracken, J.J. Elser, D.S. Gruner, H. Hillebrand, J.B. Shurin, and J.E. Smith. 2011. Nutrient co-limitation of primary producer communities. Ecol Lett 14: 852–862.

    Article  Google Scholar 

  • Harris, H. 1989. The human alkaline phosphatases: what we know and what we don’t know. Clin. Chim. Acta 186: 133–150.

    Article  Google Scholar 

  • Harrison, P.J., H.L. Conway, and R.C. Dugdale. 1976. Marine diatoms grown in chemostats under silicate or ammonium limitation. I. Cellular chemical composition and steady-state growth kinetics of Skeletonema costatum. Mar. Biol 35: 177–186.

    Article  CAS  Google Scholar 

  • Harrison, P.J., M.H. Hu, Y.P. Yang, and X. Lu. 1990. Phosphate limitation in estuarine and coastal waters of China. J. of Exp. Mar. Biol. Ecol 140: 79–87.

    Article  CAS  Google Scholar 

  • Huang, Z., W. You, R.P. Haugland, V.B. Paragas, N.A. Olson, and R.P. Haugland. 1993. A novel fluorogenic substrate for detecting alkaline phosphatase activity in situ. J Histochem Cytochem 41: 313–317.

    Article  CAS  Google Scholar 

  • Healey, R.P., and L.L. Hendzel. 1980. Physiological indicators of nutrient deficiency in lake phytoplankton. Can J Fish Aquat Sci 37: 442–453.

    Article  CAS  Google Scholar 

  • Hessle, L., K.A. Johnson, H.C. Anderson, S. Narisawa, A. Sali, J.W. Goding, R. Terkeltaub, and J.L. Millán. 2002. Tissue-nonspecific alkaline phosphatase and plasma cell membrane glycoprotein-1 are central antagonistic regulators of bone mineralization. Proc Natl Acad Sci U S A 99: 9445–9449.

    Article  CAS  Google Scholar 

  • Howarth, R.W. 1988. Nutrient limitation of net primary production in marine ecosystems. Ann. Rev. Ecol. Syst 19: 89–110.

    Article  Google Scholar 

  • Kathurla, S., and A.C. Martiny. 2011. Prevalence of a calcium-based alkaline phosphatase associated with the marine cyanobacterium Prochlorococcus and other ocean bacteria. Envir. Microbiol 13: 74–83.

    Google Scholar 

  • Kiššová, I., L.T. Plamondon, L. Brisson, M. Priault, V. Renouf, J. Schaeffer, N. Camougrand, and S. Manon. 2006. Evaluation of the roles of apoptosis, autophagy and mitophagy in the loss of plating efficiency induced by bax expression in yeast. J Biol Chem 281: 36187–36197.

    Article  Google Scholar 

  • Koopman, G., C.P. Reutelingsperger, G.A. Kuijten, R.M. Keehnen, S.T. Pals, and M.H. van Oers. 1994. AnnexinV for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84: 1415–1420.

    CAS  Google Scholar 

  • Kuenzler, E.J., and J.P. Perras. 1965. Phosphatase of marine algae. Biol Bull 128: 271–284.

    Google Scholar 

  • Kumar, N.A., V.N.R. Rao, and R. Rengasamy. 2009. Size differential growth and uptake kinetics of inorganic phosphate in some marine diatoms. Journal of Phytology 1: 75–85.

    CAS  Google Scholar 

  • Li, H., M.J.W. Veldhuis, and A.F. Post. 1998. Alkaline phosphatase activities among planktonic communities in the Northern Red Sea. Mar Ecol Prog Ser 173: 107–115.

    Article  Google Scholar 

  • Lippemeier, S., P. Hartig, and F. Colijn. 1999. Direct impact of silicate on the photosynthetic performance of the diatom Thalassiosira weissflogii assessed by on- and off-line PAM fluorescence measurements. J Plankton Res 21: 269–283.

    Article  Google Scholar 

  • Martin-Jézéquel, V., M. Hildebrand, and M.A. Brzezinski. 2000. Silicon metabolism in diatoms: implications for growth. J Phycol 36: 821–840.

    Article  Google Scholar 

  • Martin-Jézéquel, V., and P.J. Lopez. 2003. Silicon—a central metabolite for diatom growth and morphogenesis. Prog Mol Subcell Biol 33: 99–124.

    Article  Google Scholar 

  • Meseck, S.L., J.H. Alix, G.H. Wikfors, and J.E. Ward. 2009. Differences in the soluble, residual phosphate concentrations at which coastal phytoplankton species up-regulate alkaline-phosphatase expression, as measured by flow-cytometric detection of positive ELF-97® fluorescence. Estuar. Coast 32: 1195–1204.

    Article  CAS  Google Scholar 

  • Milligan, A.J., and F.M.M. Morel. 2002. A proton buffering role for silica in diatoms. Science 297: 1848–1850.

    Article  CAS  Google Scholar 

  • Nausch, M. 1998. Alkaline phosphatase activities and the relationship to inorganic phosphate in the Pomeranian Bight (southern Baltic Sea). Aquat Microb Ecol 16: 87–94.

    Article  Google Scholar 

  • Nauch, M., G. Nausch, and N. Wasmund. 2004. Phosphorus dynamics during the transition from nitrogen to phosphate limitation in the central Baltic Sea. Mar Ecol Prog Ser 266: 15–25.

    Article  Google Scholar 

  • Nicholson, D., S. Dyhrman, F. Chavez, and A. Paytan. 2006. Alkaline phosphate activity in the phytoplankton communities of Monterey Bay and San Francisco Bay. Limnol Oceanogr 51: 874–883.

    Article  Google Scholar 

  • Palenik, B., and S.T. Dyhrman. 1998. Recent progress in understanding the regulation of marine primary production by phosphorus. In Phosphorus in plant biology: regulating roles in molecular, cellular, organismic and ecosystem processes, ed. J.P. Lynch and J. Diekman, 26–38. Rockville: American Society of Plant Physiologists.

    Google Scholar 

  • Perry, M.J. 1972. Alkaline phosphatase activity in subtropical Central North Pacific waters using a sensitive fluorometric method. Mar Biol 15: 113–119.

    Article  CAS  Google Scholar 

  • Petterson, K. 1980. Alkaline phosphatase activity and algal surplus phosphorus as phosphorus-deficiency indicators in Lake Erken. Arch Hydrobiol 89: 54–87.

    Google Scholar 

  • Ponirakis, G., and J.E. Gough. 2006. The effects of sodium trisilicate on bone resorption and healing. Eur. Cells Mater 11: 27.

    Google Scholar 

  • Posen, S. 1967. Alkaline phosphatase. Ann. Inter. Med 67: 183–203.

    Article  CAS  Google Scholar 

  • Räike, A., O.-P. Pietiläinen, S. Rekolainen, P. Kauppila, H. Pitkänen, J. Niemi, A. Raateland, and J. Vuorenmaa. 2003. Trends of phosphorus, nitrogen and chlorophyll a concentrations in Finnish rivers and lakes in 1975–2000. Sci Total Environ 310: 47–59.

    Article  Google Scholar 

  • Rengefors, K., K. Pettersson, T. Blenckner, and D.M. Anderson. 2001. Species-specific alkaline phosphatase activity in freshwater spring phytoplankton: application of a novel method. J Plankton Res 23: 435–443.

    Article  CAS  Google Scholar 

  • Rengefors, K., K.C. Ruttenburg, C.L. Haupert, C. Taylor, B.L. Howes, and D.M. Anderson. 2003. Experimental investigation of taxon-specific response of alkaline phosphatase activity in natural freshwater phytoplankton. Limnol Oceanogr 48: 1167–1175.

    Article  CAS  Google Scholar 

  • Reynolds, C.S. 2006. The ecology of phytoplankton. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Richthammer, P., M. Börmel, M.E. Brunner, and K. van Pée. 2011. Biomineralization in diatoms: the role of silacidins. ChemBioChem 12: 1362–1366.

    Article  CAS  Google Scholar 

  • Roy, N.K., R.K. Ghosh, and J. Das. 1982. Monomeric alkaline phosphatase of Vibrio cholerae. J Bacteriol 150: 1033–1039.

    CAS  Google Scholar 

  • Rueter, J.G., and F.M.M. Morel. 1981. The interaction between zinc deficiency and copper toxicity as it affects the silicic acid uptake mechanisms in Thalassiosira pseudonana. Limnol Oceanogr 26: 67–73.

    Article  CAS  Google Scholar 

  • Rueter, J.G. 1983. Alkaline phosphatase limitation by copper: implications for phosphorus nutrition and use as a biochemical marker. Limnol Oceanogr 28: 743–748.

    Article  CAS  Google Scholar 

  • Sahin, K., M. Onderci, N. Sahin, T.A. Balci, M.F. Gursu, V. Jutura, and O. Kucuk. 2006. Dietary arginine silicate inositol complex improves bone mineralization in quail. Poultry Sci. 85: 486–492.

    Article  CAS  Google Scholar 

  • Schindler, D.W. 1977. Evolution of phosphorus limitation in lakes. Science 195: 260–262.

    Article  CAS  Google Scholar 

  • Sebastián, M., J.A. Aristegui, M.F. Montero, and F.X. Niell. 2004. Kinetics of alkaline phosphatase activity and effects of phosphate enrichment a case study in the NW African upwelling region. Mar Ecol Prog Ser 270: 1–13.

    Article  Google Scholar 

  • Singer, V.L., V.B. Paragas, K.D. Larison, K.S. Wells, C.J. Fox, and R.P. Haugland. 1994. Fluorescence-based signal amplification technology. Am Biothechnol Lab 12: 55–58.

  • Solórzano, L., and J.H. Sharp. 1980. Determination of total dissolved phosphorus and particulate phosphorus in natural waters. Limnol Oceanogr 24: 754–758.

    Article  Google Scholar 

  • Sullivan, C.W., and B.E. Volcani. 1973. Role of silicon in diatom metabolism II. Endogenous nucleoside triphosphate pools during silicic acid starvation of synchronized Cylindrotheca fusiformis. Biochem. Biophys. Acta 308: 205–211.

    CAS  Google Scholar 

  • Sumper, M., and E. Brunner. 2008. Silica biomineralisation in diatoms: the model organism Thalassiosira pseudonana. ChemBioChem 9: 1187–1194.

    Article  CAS  Google Scholar 

  • Sylvan, J.B., A. Quigg, S. Tozzi, and J.W. Ammerman. 2011. Mapping phytoplankton community physiology on a river impacted continental shelf: testing a multifaceted approach. Estuaries and Coasts 34: 1220–1233.

    Article  CAS  Google Scholar 

  • Torriani, A. 1960. Influence of organic phosphate in the formation of phosphatases by Escherichia coli. Biochim Biophys Acta 38: 460–479.

    Article  CAS  Google Scholar 

  • Vardi, A., I. Berman-Frank, T. Rozenberg, O. Hadas, A. Kaplan, and A. Levine. 1999. Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO2 limitation and oxidative stress. Curr Biol 9: 1061–1064.

    Article  CAS  Google Scholar 

  • Waymire, K.G., J.D. Mahuren, J.M. Jaje, T.R. Guilarte, S.P. Coburn, and G.R. MacGregor. 1995. Mice lacking tissue non-specific alkaline phosphatase die from seizures due to defective metabolism of vitamin B-6. Nat Genet 2: 45–51.

    Article  Google Scholar 

  • Werner, D. 1966. Die Kieselsaure im Stoffwechsel von Cyclotella cryptica Reimann, Lewin und Guil- lard. Arch. Mikrobiol. 55: 278–308.

    Article  CAS  Google Scholar 

  • Wick, M.R., P.E. Swanson, and J.C. Manivel. 1987. Placental-like alkaline phosphatase reactivity in human tumors: an immunohistochemical study of 520 cases. Hum Pathol 18: 946–954.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yamaguchi, H., M. Yamaguchi, and M. Adachi. 2006. Specific-detection of alkaline phosphatase activity in individual species of marine phytoplankton. Plankton Benthos Res 4: 214–217.

    Article  Google Scholar 

  • Zohar, T., and R.D. Robarts. 1998. Experimental study of microbial P limitation in the eastern Mediterranean. Limnol Oceanogr 43: 387–395.

    Article  Google Scholar 

Download references

Acknowledgments

We thank Jennifer H. Alix and Kimberly Dickinson, for their assistance during the experiment. This worked was supported by the NOAA Aquaculture Program through the National Research Council Postdoctoral Associateship Program.

Author information

Authors and Affiliations

  1. Department of Commerce, National Oceanographic and Atmospheric Administration/NMFS, 212 Rogers Avenue, Milford, CT, 06460, USA

    Soledad Fuentes, Gary H. Wikfors & Shannon Meseck

  2. Algenol Biofuels, 16121 Lee Rd, Fort Myers, FL, 33912, USA

    Soledad Fuentes

Authors
  1. Soledad Fuentes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gary H. Wikfors
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shannon Meseck
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shannon Meseck.

Additional information

Communicated by Pat Glibert

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fuentes, S., Wikfors, G.H. & Meseck, S. Silicon Deficiency Induces Alkaline Phosphatase Enzyme Activity in Cultures of Four Marine Diatoms. Estuaries and Coasts 37, 312–324 (2014). https://doi.org/10.1007/s12237-013-9695-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-013-9695-z

Keywords

Search

Navigation