Photosynthetic activity of Prorocentrum donghaiense Lu acclimated to phosphorus limitation and its photosynthetic responses to nutrient depletion

  • Kai-Ming Sun
  • Ming Xin
  • Ping SunEmail author
  • Yan Li
  • Ruixiang Li
  • Xuexi Tang
  • Zongling Wang


Prorocentrum donghaiense blooms periodically occur in late spring and early summer in the phosphorus (P)-limited East China Sea; however, few studies have been conducted in nutrient conditions that resembled those in the East China Sea. To study the actual photosynthetic status of P. donghaiense in P-limited conditions, we established stable P-limited conditions using semi-continuous culture at two dilution rates (0.1 and 0.3 day−1). When the external nutrient concentrations remained steady after 26 days, time did not affect the maximum quantum yield (Fv/Fm), normalized Stern-Volmer quenching (NPQNSV), maximum light use efficiency (α), maximum relative electron transport rate (rETRmax), and light saturation intensity (Ik). Prorocentrum donghaiense acclimated to P limitation, and the high actual quantum yield of photosystem II (ΦPSII) and rETRmax, low NPQNSV at 0.3 day−1, and increased ΦPSII with time at 0.3 day−1 indicated the photosynthetic advantages of P. donghaiense at a high growth rate. To test the responses of P-limitation-acclimated P. donghaiense to nutrient inputs, nutrient-addition experiments were conducted. Nitrate and phosphate addition thoroughly depleted P or nitrogen (N). Greater decreases in Fv/Fm, ΦPSII, α and rETRmax, and higher NPQNSV derived from rapid light curves (RLCs) were found under the P-depletion condition than under the N depletion condition. These results showed that the P-limitation-acclimated P. donghaiense had a weaker photosynthetic tolerance to P depletion. Given the differences in the photosynthetic tolerance of P. donghaiense to nutrient depletion, our results suggested that reduced P inputs should be considered during the management of P. donghaiense blooms.


Prorocentrum donghaiense Phosphorus limitation Nutrient depletion Fv/Fm Non-photochemical quenching Rapid light curves 



We thank two anonymous reviewers for their helpful comments. We would like to express our utmost appreciation and respect to the late Prof Mingyuan Zhu in the First Institute of Oceanography, State Oceanic Administration (SOA) for his valuable suggestions on the semi-continuous algal culture. This work was supported by the National Natural Science Foundation of China (No. 41506191).


  1. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113CrossRefGoogle Scholar
  2. Beardall J, Young E, Roberts S (2001) Approaches for determining phytoplankton nutrient limitation. Aquat Sci 63:44–69CrossRefGoogle Scholar
  3. Bi R, Arndt C, Sommer U (2012) Stoichiometric responses of phytoplankton species to the interactive effect of nutrient supply ratios and growth rates. J Phycol 48:539–549CrossRefGoogle Scholar
  4. Bonnet S, Guieu C, Bruyant F, Prášil O, van Wambeke F, Raimbault P, Moutin T, Grob C, Gorbunov MY, Zehr JP, Masquelier SM, Garczarek L, Claustre H (2008) Nutrient limitation of primary productivity in the Southeast Pacific (BIOSOPE cruise). Biogeosciences 5:215–225CrossRefGoogle Scholar
  5. Browning T, Bouman H, Moore C, Schlosser C, Tarran G, Woodward E, Henderson G (2014) Nutrient regimes control phytoplankton ecophysiology in the South Atlantic. Biogeosciences 11:463–479CrossRefGoogle Scholar
  6. Browning TJ, Achterberg EP, Rapp I, Engel A, Bertrand EM, Tagliabue A, Moore CM (2017) Nutrient co-limitation at the boundary of an oceanic gyre. Nature 551:242PubMedGoogle Scholar
  7. Falkowski PG, Raven J (2007) Aqautic photosynthesis, 2nd edn. Princeton University, PrincetonGoogle Scholar
  8. García-Cañedo JC, Cristiani-Urbina E, Flores-Ortiz CM, Ponce-Noyola T, Esparza-García F, Cañizares-Villanueva RO (2016) Batch and fed-batch culture of Scenedesmus incrassatulus: effect over biomass, carotenoid profile and concentration, photosynthetic efficiency and non-photochemical quenching. Algal Res 13:41–52CrossRefGoogle Scholar
  9. General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China, Standardization Administration of the People’s Republic of China (2007) Specifications for oceanographic survey-Part 4: Survey of chemical parameters in sea water. Standards Press of China, BeijingGoogle Scholar
  10. Glibert PM, Burkholder JM, Kana TM (2012) Recent insights about relationships between nutrient availability, forms, and stoichiometry, and the distribution, ecophysiology, and food web effects of pelagic and benthic Prorocentrum species. Harmful Algae 14:231–259CrossRefGoogle Scholar
  11. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals: proceedings — 1st conference on culture of marine invertebrate animals Greenport. Springer, New York, pp 29–60CrossRefGoogle Scholar
  12. Guo S, Feng Y, Wang L, Dai M, Liu Z, Bai Y, Sun J (2014) Seasonal variation in the phytoplankton community of a continental-shelf sea: the East China Sea. Mar Ecol Prog Ser 516:103–126CrossRefGoogle Scholar
  13. Halsey KH, Milligan AJ, Behrenfeld MJ (2010) Physiological optimization underlies growth rate-independent chlorophyll-specific gross and net primary production. Photosynth Res 103:125–137CrossRefGoogle Scholar
  14. Harrison JW, Smith RE (2013) Effects of nutrients and irradiance on PSII variable fluorescence of lake phytoplankton assemblages. Aquat Sci 75:399–411CrossRefGoogle Scholar
  15. Heinz Walz GmbH (2003) Phytoplankton analyzer Phyto-PAM and Phyto-Win software V 1.45, system components and principles of operation, 2nd edn. Heinz Walz GmbH, GermanyGoogle Scholar
  16. Hu Z, Mulholland MR, Duan S, Xu N (2012) Effects of nitrogen supply and its composition on the growth of Prorocentrum donghaiense. Harmful Algae 13:72–82CrossRefGoogle Scholar
  17. Huang X, Huang B, Chen J, Liu X (2016) Cellular responses of the dinoflagellate Prorocentrum donghaiense Lu to phosphate limitation and chronological ageing. J Plankton Res 38:83–93CrossRefGoogle Scholar
  18. Hughes DJ, Varkey D, Doblin MA, Ingleton T, Mcinnes A, Ralph PJ, van Dongen-Vogels V, Suggett DJ (2018) Impact of nitrogen availability upon the electron requirement for carbon fixation in Australian coastal phytoplankton communities. Limnol Oceanogr 63:1891–1910CrossRefGoogle Scholar
  19. Jiang Z, Chen J, Zhou F, Shou L, Chen Q, Tao B, Yan X, Wang K (2015) Controlling factors of summer phytoplankton community in the Changjiang (Yangtze River) Estuary and adjacent East China Sea shelf. Cont Shelf Res 101:71–84CrossRefGoogle Scholar
  20. Kruskopf M, Flynn KJ (2006) Chlorophyll content and fluorescence responses cannot be used to gauge reliably phytoplankton biomass, nutrient status or growth rate. New Phytol 169:525–536CrossRefGoogle Scholar
  21. Li J, Sun X (2016) Effects of different phosphorus concentrations and N/P ratios on the growth and photosynthetic characteristics of Skeletonema costatum and Prorocentrum donghaiense. Chin J Oceanol Limnol 34:1158–1172CrossRefGoogle Scholar
  22. Li J, Glibert PM, M-j Z, Lu S, Lu D (2009) Relationships between nitrogen and phosphorus forms and ratios and the development of dinoflagellate blooms in the East China Sea. Mar Ecol Prog Ser 383:11–26CrossRefGoogle Scholar
  23. Li J, Glibert PM, Zhou M (2010) Temporal and spatial variability in nitrogen uptake kinetics during harmful dinoflagellate blooms in the East China Sea. Harmful Algae 9:531–539CrossRefGoogle Scholar
  24. Li H-M, Tang H-J, Shi X-Y, Zhang C-S, Wang X-L (2014) Increased nutrient loads from the Changjiang (Yangtze) River have led to increased harmful algal blooms. Harmful Algae 39:92–101CrossRefGoogle Scholar
  25. Liu S, Guo Z, Li T, Huang H, Lin S (2011) Photosynthetic efficiency, cell volume, and elemental stoichiometric ratios in Thalassirosira weissflogii under phosphorus limitation. Chin J Oceanol Limnol 29:1048–1056CrossRefGoogle Scholar
  26. Liu X, Beusen AH, Van Beek LP, Mogollón JM, Ran X, Bouwman AF (2018) Exploring spatiotemporal changes of the Yangtze River (Changjiang) nitrogen and phosphorus sources, retention and export to the East China Sea and Yellow Sea. Water Res 142:246–255CrossRefGoogle Scholar
  27. Lu D, Goebel J, Qi Y, Zou J, Han X, Gao Y, Li Y (2005) Morphological and genetic study of Prorocentrum donghaiense Lu from the East China Sea, and comparison with some related Prorocentrum species. Harmful Algae 4:493–505CrossRefGoogle Scholar
  28. Ly J, Philippart CJ, Kromkamp JC (2014) Phosphorus limitation during a phytoplankton spring bloom in the western Dutch Wadden Sea. J Sea Res 88:109–120CrossRefGoogle Scholar
  29. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668CrossRefGoogle Scholar
  30. McKew BA et al (2013) The trade-off between the light-harvesting and photoprotective functions of fucoxanthin-chlorophyll proteins dominates light acclimation in Emiliania huxleyi (clone CCMP 1516). New Phytol 200:74–85CrossRefGoogle Scholar
  31. Napoléon C, Raimbault V, Claquin P (2013) Influence of nutrient stress on the relationships between PAM measurements and carbon incorporation in four phytoplankton species. PLoS One 8:e66423CrossRefGoogle Scholar
  32. Ou L, Wang D, Huang B, Hong H, Qi Y, Lu S (2008) Comparative study of phosphorus strategies of three typical harmful algae in Chinese coastal waters. J Plankton Res 30:1007–1017CrossRefGoogle Scholar
  33. Ou L, Huang B, Hong H, Qi Y, Lu S (2010) Comparative alkaline phosphatase characteristics of the algal bloom dinoflagellates Prorocentrun donghaiense and Alexandrium catanella, and the diatom Skeletonema costatum. J Phycol 46:260–265CrossRefGoogle Scholar
  34. Oxborough K (2012) FastPro8 GUI and FRRf3 systems documentation. Chelsea Technologies Group LtdGoogle Scholar
  35. Parkhill JP, Maillet G, Cullen JJ (2001) Fluorescence-based maximal quantum yield for PSII as a diagnostic of nutrient stress. J Phycol 37:517–529CrossRefGoogle Scholar
  36. Petrou K, Kranz SA, Doblin MA, Ralph PJ (2012) Photophysiological responses of Fragilariopsis cylindrus (Bacillariophyceae) to nitrogen depletion at two temperatures. J Phycol 48:127–136CrossRefGoogle Scholar
  37. Qi H, Wang J, Wang Z (2013) A comparative study of maximal quantum yield of photosystem II to determine nitrogen and phosphorus limitation on two marine algae. J Sea Res 80:1–11CrossRefGoogle Scholar
  38. Qu HJ, Kroeze C (2012) Nutrient export by rivers to the coastal waters of China: management strategies and future trends. Reg Environ Chang 12:153–167CrossRefGoogle Scholar
  39. Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237CrossRefGoogle Scholar
  40. Rocha GS, Parrish CC, Lombardi AT, da Graça Gama Melão M (2018) Biochemical and physiological responses of Selenastrum gracile (Chlorophyceae) acclimated to different phosphorus concentrations. J Appl Phycol 30:2167–2177CrossRefGoogle Scholar
  41. Rodríguez-Román A, Iglesias-Prieto R (2005) Regulation of photochemical activity in cultured symbiotic dinoflagellates under nitrate limitation and deprivation. Mar Biol 146:1063–1073CrossRefGoogle Scholar
  42. Roleda MY, Mohlin M, Pattanaik B, Wulff A (2008) Photosynthetic response of Nodularia spumigena to UV and photosynthetically active radiation depends on nutrient (N and P) availability. FEMS Microbiol Ecol 66:230–242CrossRefGoogle Scholar
  43. Rosset S, Wiedenmann J, Reed AJ, D'Angelo C (2017) Phosphate deficiency promotes coral bleaching and is reflected by the ultrastructure of symbiotic dinoflagellates. Mar Pollut Bull 118:180–187CrossRefGoogle Scholar
  44. Saeck EA, Brien KRO, Burford MA (2016) Nitrogen response of natural phytoplankton communities: a new indicator based on photosynthetic efficiency F v/F m. Mar Ecol Prog Ser 552:81–92CrossRefGoogle Scholar
  45. Shelly K, Holland D, Beardall J (2010) Assessing nutrient status of microalgae using chlorophyll a fluorescence. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications. Springer, Dordrecht, pp 223–235CrossRefGoogle Scholar
  46. Shi X, Lin X, Li L, Li M, Palenik B, Lin S (2017) Transcriptomic and microRNAomic profiling reveals multi-faceted mechanisms to cope with phosphate stress in a dinoflagellate. ISME J 11:2209–2218CrossRefGoogle Scholar
  47. Sun K-M, Li R, Li Y, Tang X, Wang Z (2016) Changes of fluorescence parameters of photosynthetic system II in Prorocentrum donghaiense Lu during population growth. Mar Environ Sci 35:226–230 (in Chinese with English abstract)Google Scholar
  48. Sutherland DL, Turnbull MH, Broady PA, Craggs RJ (2014) Effects of two different nutrient loads on microalgal production, nutrient removal and photosynthetic efficiency in pilot-scale wastewater high rate algal ponds. Water Res 66:53–62CrossRefGoogle Scholar
  49. Wang Z, Wang J, Tan L (2014) Variation in photosynthetic activity of phytoplankton during the spring algal blooms in the adjacent area of Changjiang River estuary. Ecol Indic 45:465–473CrossRefGoogle Scholar
  50. Xu N, Duan S, Li A, Zhang C, Cai Z, Hu Z (2010) Effects of temperature, salinity and irradiance on the growth of the harmful dinoflagellate Prorocentrum donghaiense Lu. Harmful Algae 9:13–17CrossRefGoogle Scholar
  51. Yu Y, Wang P, Wang C, Wang X (2018) Optimal reservoir operation using multi-objective evolutionary algorithms for potential estuarine eutrophication control. J Environ Manag 223:758–770CrossRefGoogle Scholar
  52. Zhang YJ, Zhang SF, He ZP, Lin L, Wang DZ (2015) Proteomic analysis provides new insights into the adaptive response of a dinoflagellate Prorocentrum donghaiense to changing ambient nitrogen. Plant Cell Environ 38:2128–2142CrossRefGoogle Scholar
  53. Zhao Y, Wang Y, Quigg A (2015a) Comparison of population growth and photosynthetic apparatus changes in response to different nutrient status in a diatom and a coccolithophore. J Phycol 51:872–884CrossRefGoogle Scholar
  54. Zhao Y, Wang Y, Quigg A (2015b) The 24 hour recovery kinetics from N starvation in Phaeodactylum tricornutum and Emiliania huxleyi. J Phycol 51:726–738CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Kai-Ming Sun
    • 1
    • 2
    • 3
  • Ming Xin
    • 1
  • Ping Sun
    • 1
    • 2
    • 4
    Email author
  • Yan Li
    • 1
  • Ruixiang Li
    • 1
  • Xuexi Tang
    • 3
  • Zongling Wang
    • 1
  1. 1.First Institute of OceanographyMinistry of Natural ResourcesQingdaoPeople’s Republic of China
  2. 2.Laboratory of Marine Ecology and Environmental ScienceQingdao National Laboratory for Marine Science and TechnologyQingdaoPeople’s Republic of China
  3. 3.College of Marine LifeOcean University of ChinaQingdaoPeople’s Republic of China
  4. 4.College of Environmental Science and EngineeringOcean University of ChinaQingdaoPeople’s Republic of China

Personalised recommendations