, Volume 765, Issue 1, pp 197–207 | Cite as

Effects of turbulence on alkaline phosphatase activity of phytoplankton and bacterioplankton in Lake Taihu

  • Jian Zhou
  • Boqiang QinEmail author
  • Céline Casenave
  • Xiaoxia Han
Primary Research Paper


Alkaline phosphatase (AP), an inducible and hydrolytic enzyme, plays a key role in the biogeochemical cycle of phosphorus (P) in lakes. Activity and regulation of AP has been suggested to be affected by hydrodynamic turbulence. However, many aspects of the coupling of the AP activity (APA) and turbulence are still to be investigated and understood. In this study, mesocosm experiments were carried out to further understand the effects of turbulence on APA and the relative contribution of the different microbial groups to the total APA (TAPA). Specifically, we focused on evaluating the APA of phytoplankton (2–112 µm) and bacterioplankton (0.2–2 µm) and its relationship with P fractions under four turbulence levels. Results showed that turbulent conditions enhanced planktonic APA (PAPA) which dominated TAPA by comprising 66–93% of the total fraction. In particular, PAPA was almost two times higher in the turbulence treatments than in still-water control. On the other hand, bacterioplanktonic APA (BAPA) decreased which could be associated with the competitive advantage of bacteria in nutrient-limited conditions due to surface-to-volume ratio. The results suggest that turbulence can accelerate the biogeochemical cycle of P and plays an important role in P strategies of plankton.


Turbulence Alkaline phosphatase activity Phytoplankton Bacterioplankton Phosphorus deficiency Phosphorus strategy 



We appreciate the very thorough and constructive reviews provided by two anonymous reviewers. This research was supported by the National Natural Science Foundation of China (41230744).


  1. Barton, A. D., B. A. Ward, R. G. Williams & M. J. Follows, 2014. The impact of fine-scale turbulence on phytoplankton community structure. Limnology and Oceanography: Fluids and Environments 4(1): 34–49.Google Scholar
  2. Bergstedt, M. S., M. M. Hondzo & J. B. Cotner, 2004. Effects of small scale fluid motion on bacterial growth and respiration. Freshwater Biology 49(1): 28–40.CrossRefGoogle Scholar
  3. Cao, X., C. Song & Y. Zhou, 2009a. Limitations of using extracellular alkaline phosphatase activities as a general indicator for describing P deficiency of phytoplankton in Chinese shallow lakes. Journal of Applied Phycology 22(1): 33–41.CrossRefGoogle Scholar
  4. Cao, X., C. Song, Y. Zhou, A. Štrojsová, P. Znachor, E. Zapomělová & J. Vrba, 2009b. Extracellular phosphatases produced by phytoplankton and other sources in shallow eutrophic lakes (Wuhan, China): taxon-specific versus bulk activity. Limnology 10(2): 95–104.CrossRefGoogle Scholar
  5. Cao, X., C. Song & Y. Zhou, 2010. Limitations of using extracellular alkaline phosphatase activities as a general indicator for describing P deficiency of phytoplankton in Chinese shallow lakes. Journal of Applied Phycology 22(1): 33–41.CrossRefGoogle Scholar
  6. Cardoso, L. S. & D. M. Marques, 2009. Hydrodynamics-driven plankton community in a shallow lake. Aquatic Ecology 43(1): 73–84.CrossRefGoogle Scholar
  7. Carpenter, S. R., 2008. Phosphorus control is critical to mitigating eutrophication. Proceedings of the National Academy of Sciences of the United States of America 105(32): 11039–11040.PubMedCentralCrossRefPubMedGoogle Scholar
  8. Clarke, R. D., E. J. Buskey & K. C. Marsden, 2005. Effects of water motion and prey behavior on zooplankton capture by two coral reef fishes. Marine Biology 146(6): 1145–1155.CrossRefGoogle Scholar
  9. Currie, D. J. & J. Kalff, 1984a. Can bacteria outcompete phytoplankton for phosphorus? a chemostat test. Microbial Ecology 10(3): 205–216.CrossRefPubMedGoogle Scholar
  10. Currie, D. J. & J. Kalff, 1984b. The relative importance of bacterioplankton and phytoplankton in phosphorus uptake in freshwater. Limnology and Oceanography 29(2): 311–321.CrossRefGoogle Scholar
  11. Drakare, S., 2002. Competition between picoplanktonic cyanobacteria and heterotrophic bacteria along crossed gradients of glucose and phosphate. Microbial Ecology 44(4): 327–335.CrossRefPubMedGoogle Scholar
  12. Dyhrman, S. T. & K. C. Ruttenberg, 2006. Presence and regulation of alkaline phosphatase activity in eukaryotic phytoplankton from the coastal ocean: implications for dissolved organic phosphorus remineralization. Limnology and Oceanography 51(3): 1381–1390.CrossRefGoogle Scholar
  13. Feuillade, J., M. Feuillade & P. Blanc, 1990. Alkaline phosphatase activity fluctuations and associated factors in a eutrophic lake dominated by Oscillatoria rubescens. Hydrobiologia 207(1): 233–240.CrossRefGoogle Scholar
  14. Gao, G., G. W. Zhu, B. Q. Qin, J. Chen & K. Wang, 2006. Alkaline phosphatase activity and the phosphorus mineralization rate of Lake Taihu. Science in China Series D 49: 176–185.CrossRefGoogle Scholar
  15. G.-Tóth, L., L. Parpala, C. Balogh, I. Tátrai & E. Baranyai, 2011. Zooplankton community response to enhanced turbulence generated by water-level decrease in Lake Balaton, the largest shallow lake in Central Europe. Limnology and Oceanography 56(6): 2211–2222.CrossRefGoogle Scholar
  16. Guasto, J. S., R. Rusconi & R. Stocker, 2012. Fluid mechanics of planktonic microorganisms. Annual Review of Fluid Mechanics 44(1): 373–400.CrossRefGoogle Scholar
  17. Härkönen, L., Z. Pekcan-Hekim, N. Hellén, A. Ojala & J. Horppila, 2014. Combined effects of turbulence and different predation regimes on zooplankton in highly colored water – implications for environmental change in lakes. PloS One 9(11): e111942.PubMedCentralCrossRefPubMedGoogle Scholar
  18. Hernandez, I., F. X. Niell & B. A. Whitton, 2002. Phosphatase activity of benthic marine algae. An overview. Journal of Applied Phycology 14(6): 475–487.CrossRefGoogle Scholar
  19. Honzo, M. & A. Wüest, 2008. Do microscopic organisms feel turbulent flows. Environmental Science and Technology 43: 764–768.CrossRefGoogle Scholar
  20. Istvánovics, V., 2008. The role of biota in shaping the phosphorus cycle in lakes. Freshwater Reviews 1(2): 143–174.CrossRefGoogle Scholar
  21. Ivancic, I., J. Godrijan, M. Pfannkuchen, D. Maric, B. Gasparovic, T. Djakovac & M. Najdek, 2012. Survival mechanisms of phytoplankton in conditions of stratification-induced deprivation of orthophosphate: Northern Adriatic case study. Limnology and Oceanography 57(6): 1721–1731.CrossRefGoogle Scholar
  22. Jamet, D., C. Amblard & J. Devaux, 1997. Seasonal changes in alkaline phosphatase activity of bacteria and microalgae in Lake Pavin (Massif Central, France). Hydrobiologia 347: 185–195.CrossRefGoogle Scholar
  23. Jansson, M., H. Olsson & K. Pettersson, 1988. Phosphatases; origin, characteristics and function in lakes. Hydrobiologia 170: 157–175.CrossRefGoogle Scholar
  24. Kundu, P. K. & I. M. Cohen, 2010. Fluid mechanics. San Diego Academic Press, San Diego.Google Scholar
  25. Labry, C., D. Delmas & A. Herbland, 2005. Phytoplankton and bacterial alkaline phosphatase activities in relation to phosphate and DOP availability within the Gironde plume waters (Bay of Biscay). Journal of Experimental Marine Biology and Ecology 318(2): 213–225.CrossRefGoogle Scholar
  26. Litchman, E. & B. L. V. Nguyen, 2008. Alkaline phosphatase activity as a function of internal phosphorus concentration in freshwater phytoplankton. Journal of Phycology 44(6): 1379–1383.CrossRefGoogle Scholar
  27. Meseck, S. L., J. H. Alix, G. H. Wikfors & 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 ELF-97A fluorescence. Estuaries and Coasts 32(6): 1195–1204.CrossRefGoogle Scholar
  28. Nedoma, J., J. C. Garcia, M. Comerma, K. Šimek & J. Armengol, 2006. Extracellular phosphatases in a Mediterranean reservoir: seasonal, spatial and kinetic heterogeneity. Freshwater Biology 51(7): 1264–1276.CrossRefGoogle Scholar
  29. Nu, L., W. Hu, J. Deng, S. Zhai, X. Chen & X. Zhou, 2009. Partial distribution characteristics and ecological significance of alkaline phosphatase in water column of Lake Taihu. Environmental Science 30(10): 2898–2903. (in Chinese).Google Scholar
  30. Panosso, R. & F. Esteves, 2000. Effects of disturbance on phosphorus turnover and plankton dynamics. Journal of Plankton Research 22(3): 589–595.CrossRefGoogle Scholar
  31. Pápista, É., É. Ács & B. Böddi, 2002. Chlorophyll-a determination with ethanol – a critical test. Hydroiologia 485: 191–198.CrossRefGoogle Scholar
  32. Pekcan-Hekim, Z., L. Joensuu, J. Horppila & J. Grant, 2013. Predation by a visual planktivore perch (Perca fluviatilis) in a turbulent and turbid environment. Canadian Journal of Fisheries and Aquatic Sciences 70(6): 854–859.CrossRefGoogle Scholar
  33. Peters, F. & J. M. Redondo, 1997. Turbulence generation and measurement: application to studies on plankton. Scientia Marina 61: 205–228.Google Scholar
  34. Prairie, J. C., K. R. Sutherland, K. J. Nickols & A. M. Kaltenberg, 2012. Biophysical interactions in the plankton: a cross-scale review. Limnology and Oceanography: Fluids and Environments 2: 121–145.Google Scholar
  35. Qin, B. Q., P. Z. Xu, Q. L. Wu, L. C. Luo & Y. L. Zhang, 2007. Environmental issues of Lake Taihu, China. Hydrobiologia 581: 3–14.CrossRefGoogle Scholar
  36. Qin, B. Q., G. W. Zhu, G. Gao, Y. L. Zhang, W. Li, H. W. Paerl & W. W. Carmichael, 2010. A drinking water crisis in Lake Taihu, China: linkage to climatic variability and lake management. Environmental Management 45(1): 105–112.CrossRefPubMedGoogle Scholar
  37. Raheb, J., S. Naghdi & K. P. Flint, 2006. Alkaline phosphatase activity of Flexibacter chinensis under starvation stress in water microcosms. Enzyme and Microbial Technology 40(1): 13–16.CrossRefGoogle Scholar
  38. Rengefors, K., K. Pettersson, T. Blenckner & D. M. Anderson, 2001. Species-specific alkaline phosphatase activity in freshwater spring phytoplankton: application of a novel method. Journal of Plankton Research 23(4): 435–443.CrossRefGoogle Scholar
  39. Sanford, L. P., 1997. Turbulent mixing in experimental ecosystem studies. Marine Ecology Progress Series 161: 265–293.CrossRefGoogle Scholar
  40. Tanaka, T., P. Henriksen, R. Lignell, K. Olli, J. Seppala, T. Tamminen & T. F. Thingstad, 2006. Specific affinity for phosphate uptake and specific alkaline phosphatase activity as diagnostic tools for detecting phosphorus-limited phytoplankton and bacteria. Estuaries and Coasts 29: 1226–1241.CrossRefGoogle Scholar
  41. Tanaka, T., T. F. Thingstad, T. Lovdal, H.-P. Gressart, A. Larsen, M. Allgaier, M. Meyerhöfer, K. G. Schulz, J. Wohlers, E. Zöllner & U. Riebesell, 2008. Availability of phosphate for phytoplankton and bacteria and of labile organic carbon for bacteria at different pCO2 levels in a mesocosm study. Biogeosciences 5: 669–678.CrossRefGoogle Scholar
  42. Wetzel, R. G., 2001. Limnology: lake and river ecosystems. Academic Press, New York: 85–111.Google Scholar
  43. Wu, T., B. Qin, G. Zhu, L. Luo, Y. Ding & G. Bian, 2013. Dynamics of cyanobacterial bloom formation during short-term hydrodynamic fluctuation in a large shallow, eutrophic, and wind-exposed Lake Taihu, China. Environmental Science and Pollution Research 20(12): 8546–8556.CrossRefPubMedGoogle Scholar
  44. Yockey, R. D., 2010. SPSS Demystified: A Step By Step Approach. Prentice Hall Press, Upper Saddle River.Google Scholar
  45. Zhang, T., X. Wang & X. Jin, 2007. Variations of alkaline phosphatase activity and P fractions in sediments of a shallow Chinese eutrophic lake (Lake Taihu). Environmental Pollution 150(2): 288–294.CrossRefPubMedGoogle Scholar
  46. Zhou, Y. Y. & X. Y. Zhou, 1997. Seasonal variation in kinetic parameters of alkaline phosphatase activity in a shallow Chinese freshwater lake (Donghu Lake). Water Research 31(5): 1232–1235.CrossRefGoogle Scholar
  47. Zhu, M., H. W. Paerl, G. Zhu, T. Wu, W. Li, K. Shi, L. Zhao, Y. Zhang, B. Qin & A. M. Caruso, 2014. The role of tropical cyclones in stimulating cyanobacterial (Microcystis spp.) blooms in hypertrophic Lake Taihu, China. Harmful Algae 39: 310–321.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Jian Zhou
    • 1
    • 2
  • Boqiang Qin
    • 1
    Email author
  • Céline Casenave
    • 3
  • Xiaoxia Han
    • 4
  1. 1.State Key Laboratory of Lake Science and Environment, Nanjing Institute of Geography and LimnologyChinese Academy of SciencesNanjingPeople’s Republic of China
  2. 2.University of Chinese Academy of SciencesBeijingPeople’s Republic of China
  3. 3.UMR INRA-SupAgro 0729 MISTEA (Mathematics, Informatics and Statistics for Environment & Agronomy)MontpellierFrance
  4. 4.College of Resources and Environmental SciencesNanjing Agricultural UniversityNanjingPeople’s Republic of China

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