Skip to main content
Log in

Nutritional strategy for the preferential uptake of \({{\text{NO}}_{3}}^{ - } {\text{{-}N}}\) by Phaeocystis globosa

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The cosmopolitan alga Phaeocystis globosa forms massive colonies during blooms. In addition to producing haemolytic toxins that affect the ecosystem, centimetre-sized colonies can block nuclear power plant cooling systems. Nitrogen plays a key role in P. globosa blooms; however, the preferred form of inorganic nitrogen taken up by colonies remains unknown. Therefore, we set up four groups with different nitrogen types and levels of enrichment. The culture medium and intracolonial fluid were sampled at different times for the determination of nutrient concentrations to elucidate the nutrient uptake strategy that presumably favours colonies. Although \({{\text{NH}}_{4}}^{ + } {\text{ {-} N}}\) and \({{\text{NO}}_{2}}^{ - } {\text{{-}N}}\) were absorbed by the colonies, \({{\text{NO}}_{3}}^{ - } {\text{{-}N}}\) was the favoured nitrogen, and the average uptake rate of \({{\text{NO}}_{3}}^{ - } {\text{{-}N}}\) was significantly higher than that of \({{\text{NH}}_{4}}^{ + } {\text{{-}N}}\) and \({{\text{NO}}_{2}}^{ - } {\text{{-}N}}\) in each group (P < 0.05). In the enriched groups, the replenishment of \({{\text{NO}}_{3}}^{ - } {\text{{-}N}}\) in the intracolonial fluid was faster than that of \({{\text{NH}}_{4}}^{ + } {\text{{-}N}}\). The symbiotic bacteria and some biochemical processes may explain the differences in the nutrient concentrations inside and outside of the colonies. Considering the high consumption of \({{\text{NO}}_{3}}^{ - } {\text{{-}N}}\) during P. globosa blooms, controlling the concentration of \({{\text{NO}}_{3}}^{ - } {\text{{-}N}}\) is key to preventing P. globosa blooms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alderkamp, A. C., A. G. J. Buma & M. van Rijssel, 2007. The carbohydrates of Phaeocystis and their degradation in the microbial food web. Biogeochemistry 83: 99–118.

    Article  CAS  Google Scholar 

  • Anderson, D. M., P. M. Glibert & J. M. Burkholder, 2002. Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25: 704–726.

    Article  Google Scholar 

  • Balode, M., I. Purina, C. Beéchemin & S. Y. Maestrini, 1998. Effects of nutrient enrichment on the growth rates and community structure of summer phytoplankton from the Gulf of Riga, Baltic Sea. Journal of Plankton Research 20: 2251–2272.

    Article  CAS  Google Scholar 

  • Baudoux, A. C. & C. P. D. Brussaard, 2005. Characterization of different viruses infecting the marine harmful algal bloom species Phaeocystis globosa. Virology 341: 80–90.

    Article  CAS  PubMed  Google Scholar 

  • Baumann, M. E. M., C. Lancelot, F. P. Brandini, E. Sakshaug & D. M. John, 1994. The taxonomic identity of the cosmopolitan prymnesiophyte Phaeocystis: a morphological and ecophysiological approach. Journal of Marine Systems 5: 5–22.

    Article  Google Scholar 

  • Berman, T., 1997. Dissolved organic nitrogen utilization by an Aphanizomenon bloom in Lake Kinneret. Journal of Plankton Research 19: 577–586.

    Article  Google Scholar 

  • Cao, X., Z. Yu & L. Qiu, 2017. Field experiment and emergent application of modified clays for Phaeocystis globosa blooms mitigation. Oceanologia et Limnologia Sinica 48: 753–759. (in Chinese).

    Google Scholar 

  • Caperon, J. & D. A. Ziemann, 1976. Synergistic effects of nitrate and ammonium ion on the growth and uptake kinetics of Monochrysis lutheri in continuous culture. Marine Biology 36: 73–84.

    Article  CAS  Google Scholar 

  • Chen, S. & K. Gao, 2011. Solar ultraviolet radiation and CO2-induced ocean acidification interacts to influence the photosynthetic performance of the red tide alga Phaeocystis globosa (Prymnesiophyceae). Hydrobiologia 675: 105–117.

    Article  CAS  Google Scholar 

  • Chen, Y., N. Wang, P. Zhang, H. Zhou & L. Qu, 2002. Molecular evidence identifies bloom-forming Phaeocystis (Prymnesiophyta) from coastal waters of southeast China as Phaeocystis globosa. Biochemical Systematics and Ecology 30: 15–22.

    Article  CAS  Google Scholar 

  • Chi, L., X. Song, Y. Yuan, W. Wang, P. Zhou, X. Fan, X. Cao & Z. Yu, 2017. Distribution and key influential factors of dissolved oxygen off the Changjiang River Estuary (CRE) and its adjacent waters in China. Marine Pollution Bulletin 125: 440–450.

    Article  CAS  PubMed  Google Scholar 

  • Cole, J. J., 1982. Interactions between bacteria and algae in aquatic ecosystems. Annual Review of Ecology and Systematics 13: 291–314.

    Article  Google Scholar 

  • Dai, R., P. Wang, P. Jia, Y. Zhang, X. Chu & Y. Wang, 2016. A review on factors affecting microcystins production by algae in aquatic environments. World Journal of Microbiology and Biotechnology 32: 1–7.

    Article  CAS  Google Scholar 

  • Dortch, Q., 1990. The interaction between ammonium and nitrate uptake in phytoplankton. Marine Ecology Progress Series 61: 183–201.

    Article  CAS  Google Scholar 

  • Dortch, Q. & H. L. Conway, 1984. Interactions between nitrate and ammonium uptake: variation with growth rate, nitrogen source and species. Marine Biology 79: 151–164.

    Article  CAS  Google Scholar 

  • Hai, D. N., N. N. Lam & J. W. Dippner, 2010. Development of Phaeocystis globosa blooms in the upwelling waters of the South Central coast of Viet Nam. Journal of Marine Systems 83: 253–261.

    Article  Google Scholar 

  • Hamm, C. E., 2000. Architecture, ecology and biogeochemistry of Phaeocystis colonies. Journal of Sea Research 43: 307–315.

    Article  CAS  Google Scholar 

  • Hamm, C. E., D. A. Simson, R. Merkel & V. Smetacek, 1999. Colonies of Phaeocystis globosa are protected by a thin but tough skin. Marine Ecology Progress Series 187: 101–111.

    Article  Google Scholar 

  • He, C., S. Xu, S. Song & C. Li, 2019. The spatial-temporal distributions of heterotrophic bacteria in seawater of the northern Beibu Gulf. Acta Oceanologica Sinica 41: 94–108. (in Chinese).

    Google Scholar 

  • Hu, J., H. Zhang, L. Li, Y. Wang & M. Zhao, 2016. Seasonal changes of organic matter origins and anammox activity in the Changjiang Estuary deduced from multi-biomarkers in suspended particulates. Science China Earth Sciences 59: 1339–1352.

    Article  CAS  Google Scholar 

  • Jiang, X. & N. Jiao, 2016. Nitrate assimilation by marine heterotrophic bacteria. Science China Earth Sciences 59: 477–483.

    Article  CAS  Google Scholar 

  • Klein Breteler, W. C. M. & M. Koski, 2003. Development and grazing of Temora longicornis (Copepoda, Calanoida) nauplii during nutrient limited Phaeocystis globosa blooms in mesocosms. Hydrobiologia 491: 185–192.

    Article  Google Scholar 

  • Lancelot, C., N. Gypens, G. Billen, J. Garnier & V. Roubeix, 2007. Testing an integrated river-ocean mathematical tool for linking marine eutrophication to land use: The Phaeocystis-dominated Belgian coastal zone (Southern North Sea) over the past 50 years. Journal of Marine Systems 64: 216–228.

    Article  Google Scholar 

  • Larson, A., M. M. Kirk & D. L. Kirk, 1992. Molecular phylogeny of the volvocine flagellates. Molecular Biology & Evolution 9: 85–105.

    CAS  Google Scholar 

  • Lee, J., A. E. Parker, F. P. Wilkerson & R. C. Dugdale, 2015. Uptake and inhibition kinetics of nitrogen in Microcystis aeruginosa: results from cultures and field assemblages collected in the San Francisco Bay Delta, CA. Harmful Algae 47: 126–140.

    Article  CAS  Google Scholar 

  • Lunau, M., M. Voss, M. Erickson, C. Dziallas, K. Casciotti & H. Ducklow, 2013. Excess nitrate loads to coastal waters reduces nitrate removal efficiency: mechanism and implications for coastal eutrophication. Environmental Microbiology 15: 1492–1504.

    Article  CAS  PubMed  Google Scholar 

  • Madhupratap, M., S. Sawant & M. Gauns, 2000. A first report on a bloom of the marine prymnesiophycean, Phaeocystis globosa from the Arabian Sea. Oceanologica Acta 23: 83–90.

    Article  Google Scholar 

  • Mayers, J. J., K. J. Flynn & R. J. Shields, 2014. Influence of the N:P supply ratio on biomass productivity and time-resolved changes in elemental and bulk biochemical composition of Nannochloropsis sp. Bioresource Technology 169: 588–595.

    Article  CAS  PubMed  Google Scholar 

  • Nejstgaard, J. C., K. W. Tang, M. Steinke, J. Dutz, M. Koski, E. Antajan & J. D. Long, 2007. Zooplankton grazing on Phaeocystis: a quantitative review and future challenges. Biogeochemistry 83: 147–172.

    Article  Google Scholar 

  • Ohmori, M., K. Ohmori & H. Strotmann, 1977. Inhibition of nitrate uptake by ammonia in a blue-green alga, Anabaena cylindrica. Archives of Microbiology 114: 225–229.

    Article  CAS  Google Scholar 

  • Ploug, H., W. Stolte & B. B. Jørgensen, 1999. Diffusive boundary layers of the colony-forming plankton alga Phaeocystis sp.-implications for nutrient uptake and cellular growth. Limnology & Oceanography 44: 1959–1967.

    Article  CAS  Google Scholar 

  • Powell, N., A. N. Shilton, S. Pratt & Y. Chisti, 2008. Factors influencing luxury uptake of phosphorus by microalgae in waste stabilization ponds. Environmental Science & Technology 42: 5958–5962.

    Article  CAS  Google Scholar 

  • Qi, Y., J. Chen, Z. Wang, N. Xu, Y. Wang, P. Shen, S. Lu & I. J. Hodgkiss, 2004. Some observations on harmful algal bloom (HAB) events along the coast of Guangdong, southern China in 1998. Hydrobiologia 512: 209–214.

    Article  Google Scholar 

  • Riegman, R., A. A. M. Noordeloos & G. C. Cadée, 1992. Phaeocystis blooms and eutrophication of the continental coastal zones of the North Sea. Marine Biology 112: 479–484.

    Article  Google Scholar 

  • Rousseau, V., M. J. Chrétiennot-Dinet, A. Jacobsen, P. Verity & S. Whipple, 2007. The life cycle of Phaeocystis: state of knowledge and presumptive role in ecology. Biogeochemistry 83: 29–47.

    Article  Google Scholar 

  • Smith Jr., W. O., X. Liu, K. W. Tang, L. M. DeLizo, N. H. Doan, N. L. Nguyen & X. Wang, 2014. Giantism and its role in the harmful algal bloom species Phaeocystis globosa. Deep-Sea Research Part II 101: 95–106.

    Article  CAS  Google Scholar 

  • Solomonson, L. P. & M. J. Barber, 1990. Assimilatory nitrate reductase: functional properties and regulation. Annual Review of Plant Biology 41: 225–253.

    Article  CAS  Google Scholar 

  • Tan, S., X. Hu, P. Yin & L. Zhao, 2016. Photosynthetic inhibition and oxidative stress to the toxic Phaeocystis globosa caused by a diketopiperazine isolated from products of algicidal bacterium metabolism. Journal of Microbiology 54: 364–375.

    Article  CAS  PubMed  Google Scholar 

  • Tang, K. W., 2003. Grazing and colony size development in Phaeocystis globosa (Prymnesiophyceae): the role of a chemical signal. Journal of Plankton Research 25: 831–842.

    Article  Google Scholar 

  • Tang, D. L., H. Kawamura, H. Doan-Nhu & W. Takahashi, 2004. Remote sensing oceanography of a harmful algal bloom off the coast of southeastern Vietnam. Journal of Geophysical Research 109: 1–7.

    Google Scholar 

  • Terry, K. L., 1982. Nitrate uptake and assimilation in Thalassiosira weissflogii and Phaeodactylum tricornutum: interactions with photosynthesis and with the uptake of other ions. Marine Biology 69: 21–30.

    Article  CAS  Google Scholar 

  • Van Boekel, W. H. M. & M. J. W. Veldhuis, 1990. Regulation of alkaline phosphatase synthesis in Phaeocystis sp. Marine Ecology Progress Series 61: 281–289.

    Article  Google Scholar 

  • Van Rijssel, M., I. Janse, D. J. B. Noordkamp & W. W. C. Gieskes, 2000. An inventory of factors that affect polysaccharide production by Phaeocystis globosa. Journal of Sea Research 43: 297–306.

    Article  Google Scholar 

  • Veldhuis, M. J. W., C. P. D. Brussaard & A. A. M. Noordeloos, 2005. Living in a Phaeocystis colony: a way to be a successful algal species. Harmful Algae 4: 841–858.

    Article  Google Scholar 

  • Wan, X. S., H. X. Sheng, M. Dai, Y. Zhang, D. Shi, T. W. Trull, Y. Zhu, M. W. Lomas & S. J. Kao, 2018. Ambient nitrate switches the ammonium consumption pathway in the euphotic ocean. Nature Communications 9: 1–9.

    Article  CAS  Google Scholar 

  • Wang, Y., H. Tang, L. Jiang & S. Li, 2006. Effects of nitrate on the growth and nitrate reductase activity in Phaeocystis globosa. Chinese Bulletin of Botany 23: 138–144. (in Chinese).

    Google Scholar 

  • Wang, X., Y. Wang & W. O. Smith Jr., 2011. The role of nitrogen on the growth and colony development of Phaeocystis globosa (Prymnesiophyceae). European Journal of Phycology 46: 305–314.

    Article  CAS  Google Scholar 

  • Wang, W., Z. Yu, X. Song, Y. Yuan, Z. Wu, P. Zhou & X. Cao, 2018. Intrusion pattern of the offshore kuroshio branch current and its effects on nutrient contributions in the East China Sea. Journal of Geophysical Research Oceans 123: 1–13.

    Article  CAS  Google Scholar 

  • Xu, X., Z. Yu, L. He, F. Cheng, X. Cao & X. Song, 2017. Nano- and microphytoplankton community characteristics in brown tide bloom-prone waters of the Qinhuangdao coast, Bohai Sea, China. Science China Earth Sciences 60: 1189–1200.

    Article  CAS  Google Scholar 

  • Yu, Z., X. Song, X. Cao & Y. Liu, 2017. Mitigation of harmful algal blooms using modified clays: theory, mechanisms, and applications. Harmful Algae 69: 48–64.

    Article  PubMed  Google Scholar 

  • Zhang, H., Y. Peng, S. Zhang, G. Cai, Y. Li, X. Yang, K. Yang, Z. Chen, J. Zhang, H. Wang, T. Zheng & W. Zheng, 2016. Algicidal effects of prodigiosin on the harmful algae Phaeocystis globosa. Frontiers in Microbiology 7: 1–10.

    Google Scholar 

Download references

Acknowledgements

We thank the Guangxi Academy of Sciences and Guangxi Fangchenggang Nuclear Power Co., Ltd., for instrument employed. The authors sincerely thank Dr. Wentao Wang and Liyan He from Institute of Oceanology, Chinese Academy of Sciences, Qingdao for their valuable and constructive suggestions, which helped us to considerably improve the manuscript. This work was supported by the National Key Research and Development Program of China (2017YFC1404300), the National Natural Science Foundation of China (41706133), the Aoshan Talents Cultivation Program supported by Qingdao National Laboratory for Marine Science and Technology (2017ASTCP-OS16), the NSFC-Shandong Joint Fund for Marine Science Research Centers (U1606404), and the Taishan Scholars Climbing Program of Shandong Province of the year 2019.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhiming Yu.

Additional information

Handling editor: Judit Padisák

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lv, X., Wu, Z., Song, X. et al. Nutritional strategy for the preferential uptake of \({{\text{NO}}_{3}}^{ - } {\text{{-}N}}\) by Phaeocystis globosa. Hydrobiologia 846, 109–122 (2019). https://doi.org/10.1007/s10750-019-04055-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-019-04055-6

Keywords

Navigation