Chinese Journal of Oceanology and Limnology

, Volume 35, Issue 6, pp 1409–1416 | Cite as

Response of cellular stoichiometry and phosphorus storage of the cyanobacteria Aphanizomenon flos-aquae to small-scale turbulence

  • Zhe Li (李哲)
  • Yan Xiao (肖艳)
  • Jixiang Yang (杨吉祥)
  • Chao Li (李超)
  • Xia Gao (高遐)
  • Jinsong Guo (郭劲松)


Turbulent mixing, in particular on a small scale, affects the growth of microalgae by changing diffusive sublayers and regulating nutrient fluxes of cells. We tested the nutrient flux hypothesis by evaluating the cellular stoichiometry and phosphorus storage of microalgae under different turbulent mixing conditions. Aphanizomenon flos-aquae were cultivated in different stirring batch reactors with turbulent dissipation rates ranging from 0.001 51 m2/s3 to 0.050 58 m2/s3, the latter being the highest range observed in natural aquatic systems. Samples were taken in the exponential growth phase and compared with samples taken when the reactor was completely stagnant. Results indicate that, within a certain range, turbulent mixing stimulates the growth of A. flos-aquae. An inhibitory effect on growth rate was observed at the higher range. Photosynthesis activity, in terms of maximum effective quantum yield of PSII (the ratio of Fv/Fm) and cellular chlorophyll a, did not change significantly in response to turbulence. However, Chl a/C mass ratio and C/N molar ratio, showed a unimodal response under a gradient of turbulent mixing, similar to growth rate. Moreover, we found that increases in turbulent mixing might stimulate respiration rates, which might lead to the use of polyphosphate for the synthesis of cellular constituents. More research is required to test and verify the hypothesis that turbulent mixing changes the diffusive sublayer, regulating the nutrient flux of cells.


Aphanizomenon flos-aquae cellular stoichiometry photosynthesis polyphosphate turbulent dissipation rate 


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  1. Ayata S D, Lévy M, Aumont O, Resplandy L, Tagliabue A, Sciandra A, Bernard O. 2014. Phytoplankton plasticity drives large variability in carbon fixation efficiency. Geophys. Res. Lett., 41(24): 8994–9000.CrossRefGoogle Scholar
  2. Dickman E M, Vanni M J, Horgan M J. 2006. Interactive effects of light and nutrients on phytoplankton stoichiometry. Oecologia, 149(4): 676–689.CrossRefGoogle Scholar
  3. Ebert U, Arrayás M, Temme N, Sommeijer B, Huisman J. 2001. Critical conditions for phytoplankton blooms. Bull. Math. Biol., 63(6): 1095–1124.CrossRefGoogle Scholar
  4. Eixler S, Karsten U, Selig U. 2006. Phosphorus storage in Chlorella vulgaris (Trebouxiophyceae, Chlorophyta) cells and its dependence on phosphate supply. Phycologia, 45(1): 53–60.CrossRefGoogle Scholar
  5. Eixler S, Selig U, Karsten U. 2005. Extraction and detection methods for polyphosphate storage in autotrophic planktonic organisms. Hydrobiologia, 533(1-3): 135–143.CrossRefGoogle Scholar
  6. Elliott J A. 2010. The seasonal sensitivity of Cyanobacteria and other phytoplankton to changes in flushing rate and water temperature. Global Change Biol., 16(2): 864–876.CrossRefGoogle Scholar
  7. Estrada M, Berdalet E. 1997. Phytoplankton in a turbulent world. Scientia Marina, 61 (S1): 125–140.Google Scholar
  8. Gallardo Rodríguez J J, Sánchez Mirón A, García Camacho F, Cerón García M C, Belarbi E H, Chisti Y, Molina Grima E. 2009. Causes of shear sensitivity of the toxic dinoflagellate Protoceratium reticulatum. Biote chnology Progress, 25(3): 792–800.CrossRefGoogle Scholar
  9. Guillard R R L. 1973. Division rates. In: Stein J R ed. Handbook of Phycological Methods. I. Culture Methods and Growth Measurements. Cambridge University Press, Cambridge. p.289–312.Google Scholar
  10. Halsey K H, Jones B M. 2015. Phytoplankton strategies for photosynthetic energy allocation. Annu. Rev. Mar. Sci., 7(1): 265–297.CrossRefGoogle Scholar
  11. Halsey K H, Milligan A J, Behrenfeld M J. 2014. Contrasting strategies of photosynthetic energy utilization drive lifestyle strategies in ecologically important picoeukaryotes. Metabolites, 4(2): 260–280.CrossRefGoogle Scholar
  12. Hondzo M, Lyn D. 1999. Quantified small-scale turbulence inhibits the growth of a green alga. Freshwater Biol ogy, 41(1): 51–61.CrossRefGoogle Scholar
  13. Hondzo M, Wüest A. 2009. Do Microscopic organisms feel turbulent flows? Environ. Sci. Technol., 43(3): 764–768.CrossRefGoogle Scholar
  14. Huisman J, Arrayás M, Ebert U, Sommeijer B. 2002. How do sinking phytoplankton species manage to persist? Am. Nat., 159(3): 245–254.CrossRefGoogle Scholar
  15. Karp-Boss L, Boss E, Jumars P A. 1996. Nutrient fluxes to planktonic osmotrophs in the presence of fluid motion. Oceanogr. Mar. Biol. Annu. Rev, 34: 71–107.Google Scholar
  16. Klausmeier C A, Litchman E, Daufresne T, Levin S A. 2008. Phytoplankton stoichiometry. Ecol. Res., 23(3): 479–485.CrossRefGoogle Scholar
  17. Leupold M, Hindersin S, Gust G, Kerner M, Hanelt D. 2013. Influence of mixing and shear stress on Chlorella vulgaris, Scenedesmus obliquus, and Chlamydomonas reinhardtii. J. Appl. Phycol., 25(2): 485–495.CrossRefGoogle Scholar
  18. Litchman E, Klausmeier C A. 2008. Trait-based community ecology of phytoplankton. Ann. Rev. Ecol. Evol. Syst., 39(1): 615–639.CrossRefGoogle Scholar
  19. Maxwell K, Johnson G N. 2000. Chlorophyll fluorescence—a practical guide. J. Exp. Bot., 51(345): 659–668.CrossRefGoogle Scholar
  20. Michels M H A, van der Goot A J, Norsker N H, Wijffels R H. 2010. Effects of shear stress on the microalgae Chaetoceros muelleri. Bioproc. Biosyst. Eng., 33(8): 921–927.CrossRefGoogle Scholar
  21. Montechiaro F, Giordano M. 2010. Compositional homeostasis of the dinoflagellate Protoceratium reticulatum grown at three different pCO2. J. Plant Physiol., 167(2): 110–113.CrossRefGoogle Scholar
  22. O’Halloran I P, Cade-Menun B J. 2008. Total and organic phosphorus. In: Carter M R, Gregorich E G eds. Soil Sampling and Methods of Analysis. 2 nd edn. CRC Press, Boca Raton.Google Scholar
  23. Padisák J, Köhler J, Hoeg S. 1999. Effect of changing flushing rates on development of late summer Aphanizomenon and Microcystis populations in a shallow lake, Müggelsee, Berlin, Germany. In: Tundisi J G, Straškraba M eds. Theoretical Reservoir Ecology and Its Applications. Backhuys Publishers, Leiden. p.411–424.Google Scholar
  24. Parkinson J A, Allen S E. 1975. A wet oxidation procedure suitable for the determination of nitrogen and mineral nutrients in biological material. Commun. Soil Sci. Plan t Anal., 6(1): 1–11.CrossRefGoogle Scholar
  25. Powell N, Shilton A N, Pratt S, Chisti Y. 2008. Factors influencing luxury uptake of phosphorus by microalgae in waste stabilization ponds. Environ. Sci. Technol., 42(16): 5958–5962.CrossRefGoogle Scholar
  26. Powell N, Shilton A, Chisti Y, Pratt S. 2009. Towards a luxury uptake process via microalgae-defining the polyphosphate dynamics. Water Res., 43(17): 4207–4213.CrossRefGoogle Scholar
  27. Reynolds C S. 2006. The Ecology of Phytoplankton. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  28. Rothschild B J, Osborn T R. 1988. Small-scale turbulence and plankton contact rates. J. Plankton Res., 10(3): 465–474.CrossRefGoogle Scholar
  29. Sterner R W, Elser J J. 2002. Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton.Google Scholar
  30. Thomas W H, Gibson C H. 1990. Effects of small-scale turbulence on microalgae. J. Appl. Phycol., 2(1): 71–77.CrossRefGoogle Scholar
  31. Thomas W H, Vernet M, Gibson C H. 1995. Effects of smallscale turbulence on photosynthesis, pigmentation, cell division, and cell size in the marine dinoflagellate Gomaulax polyedra (Dinophyceae). J. Phycol., 31(1): 50–59.CrossRefGoogle Scholar
  32. Tripathi K, Sharma N K, Kageyama H, Takabe T, Rai A K. 2013. Physiological, biochemical and molecular responses of the halophilic cyanobacterium Aphanothece halophytica to Pi-deficiency. Eur. J. Phycol., 48(4): 461–473.CrossRefGoogle Scholar
  33. Warnaars T A, Hondzo M. 2006. Small-scale fluid motion mediates growth and nutrient uptake of Selenastrum capricornutum. Freshwater Biol ogy, 51(6): 999–1015.CrossRefGoogle Scholar
  34. Wintermans J F G M, de Mots A. 1965. Spectrophotometric characteristics of chlorophylls a and b and their phenophytins in ethanol. Biochimica et Biophysica Acta (BBA)-Biophysics including Photosynthesis, 109(2): 448–453.CrossRefGoogle Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Zhe Li (李哲)
    • 1
  • Yan Xiao (肖艳)
    • 1
  • Jixiang Yang (杨吉祥)
    • 1
  • Chao Li (李超)
    • 2
  • Xia Gao (高遐)
    • 1
  • Jinsong Guo (郭劲松)
    • 1
  1. 1.CAS Key Laboratory on Reservoir Water Environment, Chongqing Institute of Green and Intelligent TechnologyChinese Academy of SciencesChongqingChina
  2. 2.State Key Laboratory of Bioreactor Engineering, College of BiotechnologyEast China University of Science and TechnologyShanghaiChina

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