Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Nutrient uptake and transporter gene expression of ammonium, nitrate, and phosphorus in Ulva linza: adaption to variable concentrations and temperatures

Abstract

An increase in the human population has caused eutrophication in shore water due to the release of nitrogen and phosphorus. Green tides caused by the proliferation of green macroalgae are an important direct consequence of eutrophication worldwide. We studied the nutrient uptake rate (NUR) and the expression of nutrient transporter genes in the green alga Ulva linza, an alga which forms green tides almost every summer in the Yellow Sea, and identified 6 nutrient transporter genes which contributed to the uptake of ammonium, nitrate, and phosphorus. Two environmental conditions, temperature and nutrient concentration, were found to significantly influence the NUR and gene expression of nutrient transporters. The optimum concentrations for uptake of ammonium, nitrate, and phosphorus were 1398.7, 710.4, and 230.7 μmol L−1 respectively, while the optimum temperature was 15 °C. Six nutrient transporter genes (amt1, amt2, and amt3 for ammonium uptake, nit for nitrate uptake, hapt, and lapt for phosphorus) were found to have an optimal working environment in terms of temperature and nutrient concentration, respectively.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. Ahmad SH, Surif M, Omar WMW, Rosli M, Nor A (2011) Nutrient uptake, growth and chlorophyll content of green seaweed, Ulva reticulata: response to different source of inorganic nutrients. Proc UMTAS 2011:542–548

  2. Ale MT, Mikkelsen JD, Meyer AS (2010) Differential growth response of Ulva lactuca to ammonium and nitrate assimilation. J Appl Phycol 23:345–351

  3. Bohorquez J, Papaspyrou S, Yufera M, van Bergeijk SA, Garcia-Robledo E, Jimenez-Arias JL, Bright M, Corzo A (2013) Effects of green macroalgal blooms on the meiofauna community structure in the Bay of Cadiz. Mar Pollut Bull 70:10–17

  4. Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T (2011) Bacterial community assembly based on functional genes rather than species. Proc Nat Acad Sci U S A 108:14288–14293

  5. Charlier RH, Morand P, Finkl CW, Thys A (2007) Green tides on the Brittany coasts. Environ Res Eng Manag 3:52–59

  6. Choi TS, Kang EJ, J-h K, Kim KY (2010) Effect of salinity on growth and nutrient uptake of Ulva pertusa (Chlorophyta) from an eelgrass bed. Algae 25:17–26

  7. Chow F (2012) Nitrate assimilation: the role of in vitro nitrate reductase assay as nutritional predictor. In: Najapour M (ed) Applied photosynthesis. InTech, Riejeka pp 105–120

  8. Crawford NM, Glass AD (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends Plat Sci 3:389–395

  9. Fan X, Xu D, Wang Y, Zhang X, Cao S, Mou S, Ye N (2014) The effect of nutrient concentrations, nutrient ratios and temperature on photosynthesis and nutrient uptake by Ulva prolifera: implications for the explosion in green tides. J Appl Phycol 26:537–544

  10. Fernandez E, Galvan A (2008) Nitrate assimilation in Chlamydomonas. Eukaryot Cell 7:555–559

  11. Flynn KJ, Clark DR, Mitra A, Fabian H, Hansen PJ, Glibert PM, Wheeler GL, Stoecker DK, Blackford JC, Brownlee C (2015) Ocean acidification with (de) eutrophication will alter future phytoplankton growth and succession. Proc R Soc B 282:20142604

  12. Galván A, Quesada A, Fernández E (1996) Nitrate and nitrite are transported by different specific transport systems and by a bispecific transporter in Chlamydomonas reinhardtii. J Biol Chem 271:2088–2092

  13. Gao G, Beardall J, Bao M, Wang C, Ren W, Xu J (2018) Ocean acidification and nutrient limitation synergistically reduce growth and photosynthetic performances of a green tide alga Ulva linza. Biogeosciences 15:3409–3420

  14. Glass AD, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat S, Siddiqi M, Unkles SE (2002) The regulation of nitrate and ammonium transport systems in plants. J Exp Bot 53:855–864

  15. Gordillo FJ, Figueroa FL, Niell FX (2003) Photon- and carbon-use efficiency in Ulva rigida at different CO2 and N levels. Planta 218:315–322

  16. Grossman A, Takahashi H (2001) Macronutrient utilization by photosynthetic eukaryotes and the fabric of interactions. Annu Rev Plant Biol 52:163–210

  17. Guttman L, Boxman SE, Barkan R, Neori A, Shpigel M (2018) Combinations of Ulva and periphyton as biofilters for both ammonia and nitrate in mariculture fishpond effluents. Algal Res 34:235–243

  18. Hepburn CD, Frew RD, Hurd CL (2011) Uptake and transport of nitrogen derived from sessile epifauna in the giant kelp Macrocystis pyrifera. Aquat Biol 14:121–128

  19. Hu C, Li D, Chen C, Ge J, Muller-Karger FE, Liu J, Yu F, He MX (2010) On the recurrent Ulva prolifera blooms in the Yellow Sea and East China Sea. J Geophys Res 115:C0517

  20. Kamer K, Boyle KA, Fong P (2001) Macroalgal bloom dynamics in a highly eutrophic southern California estuary. Estuaries 24:623–635

  21. Kim J-H, Kang EJ, Park MG, Lee B-G, Kim KY (2011) Effects of temperature and irradiance on photosynthesis and growth of a green-tide-forming species (Ulva linza) in the Yellow Sea. J Appl Phycol 23:421–432

  22. Kraiser T, Gras DE, Gutierrez AG, Gonzalez B, Gutierrez RA (2011) A holistic view of nitrogen acquisition in plants. J Exp Bot 62:1455–1466

  23. Krouk G, Crawford NM, Coruzzi GM, Tsay YF (2010) Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Biol 13:266–273

  24. Lapointe BE, Bedford BJ (2007) Drift rhodophyte blooms emerge in Lee County, Florida, USA: evidence of escalating coastal eutrophication. Harmful Algae 6:421–437

  25. Lapointe BE, Bedford BJ (2010) Ecology and nutrition of invasive Caulerpa brachypus f. parvifolia blooms on coral reefs off southeast Florida, USA. Harmful Algae 9:1–12

  26. Lapointe BE, Bedford BJ (2011) Stormwater nutrient inputs favor growth of non-native macroalgae (Rhodophyta) on O’ahu, Hawaiian Islands. Harmful Algae 10:310–318

  27. Lapointe B, Thacker K, Hanson C, Getten L (2011) Sewage pollution in Negril, Jamaica: effects on nutrition and ecology of coral reef macroalgae. Chin J Oceanol Limnol 29:775–789

  28. Leliaert F, Zhang X, Ye N, Ej M, Engelen AH, Mineur F, Verbruggen H, De Clerck O (2009) Research note: identity of the Qingdao algal bloom. Phycol Res 57:147–151

  29. Li H, Zhang Y, Tang H, Shi X, Rivkin RB, Legendre L (2017) Spatiotemporal variations of inorganic nutrients along the Jiangsu coast, China, and the occurrence of macroalgal blooms (green tides) in the southern Yellow Sea. Harmful Algae 63:164–172

  30. Liu D, Keesing JK, Xing Q, Shi P (2009) World’s largest macroalgal bloom caused by expansion of seaweed aquaculture in China. Mar Pollut Bull 58:888–895

  31. Liu D, Keesing JK, Dong Z, Zhen Y, Di B, Shi Y, Fearns P, Shi P (2010) Recurrence of the world's largest green-tide in 2009 in Yellow Sea, China: Porphyra yezoensis aquaculture rafts confirmed as nursery for macroalgal blooms. Mar Pollut Bull 60:1423–1432

  32. Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR andthe 2−ΔΔCT method. Methods 25:402–408

  33. Lotze HK, Schramm W (2000) Ecophysiological traits explain species dominance patterns in macroalgal blooms. J Phycol 36:287–295

  34. Ludewig U, Wilken S, Wu B, Jost W, Obrdlik P, El Bakkoury M, Marini AM, Andre B, Hamacher T, Boles E, von Wiren N, Frommer WB (2003) Homo- and hetero-oligomerization of ammonium transporter-1 NH4 uniporters. J Biol Chem 278:45603–45610

  35. Ludewig U, Neuhauser B, Dynowski M (2007) Molecular mechanisms of ammonium transport and accumulation in plants. FEBS Lett 581:2301–2308

  36. Luo MB, Liu F, Xu ZL (2012) Growth and nutrient uptake capacity of two co-occurring species, Ulva prolifera and Ulva linza. Aquat Bot 100:18–24

  37. Mills MM, Arrigo KR (2010) Magnitude of oceanic nitrogen fixation influenced by the nutrient uptake ratio of phytoplankton. Nat Geosci 3:412

  38. Morand P, Merceron M (2005) Macroalgal population and sustainability. J Coast Res 215:1009–1020

  39. Naldi M, Wheeler PA (1999) Changes in nitrogen pools in Ulva fenestrata (Chlorophyta) and Gracilaria pacifica (Rhodophyta) under nitrate and ammonium enrichment. J Phycol 35:70–77

  40. Neuhauser B, Dynowski M, Ludewig U (2009) Channel-like NH3 flux by ammonium transporter AtAMT2. FEBS Lett 583:2833–2838

  41. Nishikawa T, Tarutani K, Yamamoto T (2010) Nitrate and phosphate uptake kinetics of the harmful diatom Coscinodiscus wailesii, a causative organism in the bleaching of aquacultured Porphyra thalli. Harmful Algae 9:563–567

  42. Pérez-Mayorga D, Ladah L, Zertuche-González J, Leichter J, Filonov A, Lavín M (2011) Nitrogen uptake and growth by the opportunistic macroalga Ulva lactuca (Linnaeus) during the internal tide. J Exp Mar Biol Ecol 406:108–115

  43. Reis PA, Salgado MA, Vasconcelos V (2013) Seasonal variation of metal contamination in the barnacles Pollicipes pollicipes in northwest coast of Portugal show clear correlation with levels in the surrounding water. Mar Pollut Bull 70:155–161

  44. Ruiz-Marin A, Mendoza-Espinosa LG, Stephenson T (2010) Growth and nutrient removal in free and immobilized green algae in batch and semi-continuous cultures treating real wastewater. Bioresour Technol 101:58–64

  45. Runcie JW, Ritchie RJ, Larkum AW (2003) Uptake kinetics and assimilation of inorganic nitrogen by Catenella nipae and Ulva lactuca. Aquat Bot 76:155–174

  46. Shimogawara K, Wykoff DD, Usuda H, Grossman AR (1999) Chlamydomonas reinhardtii mutants abnormal in their responses to phosphorus deprivation. Plant Physiol 120:685–694

  47. Shpigel M, Guttman L, Ben-Ezra D, Yu J, Chen S (2019) Is Ulva sp. able to be an efficient biofilter for mariculture effluents? J Appl Phycol 31:2449–2459

  48. Smetacek V, Zingone A (2013) Green and golden seaweed tides on the rise. Nature 504:84–88

  49. Smith JE, Runcie JW, Smith CM (2005) Characterization of a large-scale ephemeral bloom of the green alga Cladophora sericea on the coral reefs of West Maui, Hawai'i. Mar Ecol Prog Ser 302:77–91

  50. Sohlenkamp C, Wood CC, Roeb GW, Udvardi MK (2002) Characterization of Arabidopsis AtAMT2, a high-affinity ammonium transporter of the plasma membrane. Plant Physiol 130:1788–1796

  51. Teichberg M, Fox SE, Olsen YS, Valiela I, Martinetto P, Iribarne O, Muto EY, Petti MA, Corbisier TN (2010) Eutrophication and macroalgal blooms in temperate and tropical coastal waters: nutrient enrichment experiments with Ulva spp. Glob Chang Biol 16:2624–2637

  52. Thomas TE, Harrison PJ (1987) Rapid ammonium uptake and nitrogen interactions in five intertidal seaweeds grown under field conditions. J Exp Mar Biol Ecol 107:1–8

  53. Tian R, Chen J, Sun X, Li D, Liu C, Weng H (2018) Algae explosive growth mechanism enabling weather-like forecast of harmful algal blooms. Sci Rep 8:9923

  54. Tsagkamilis P, Danielidis D, Dring MJ, Katsaros C (2009) Removal of phosphate by the green seaweed Ulva lactuca in a small-scale sewage treatment plant (Ios Island, Aegean Sea, Greece). J Appl Phycol 22:331–339

  55. Van Alstyne KL, Nelson TA, Ridgway RL (2015) Environmental chemistry and chemical ecology of “green tide” seaweed blooms. Integr Comp Biol 55:518–532

  56. van Hees DH, Van Alstyne KL (2013) Effects of emersion, temperature, dopamine, and hypoxia on the accumulation of extracellular oxidants surrounding the bloom-forming seaweeds Ulva lactuca and Ulvaria obscura. J Exp Mar Biol Ecol 448:207–213

  57. Villares R, Puente X, Carballeira A (1999) Nitrogen and phosphorus in Ulva sp. in the Galician Rias Bajas (northwest Spain): seasonal fluctuations and influence on growth. Bol Inst Esp Oceanogr 15:337–342

  58. Wang YY, Hsu PK, Tsay YF (2012) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17:458–467

  59. Wang C, Su R, Guo L, Yang B, Zhang Y, Zhang L, Xu H, Shi W, Wei L (2019) Nutrient absorption by Ulva prolifera and the growth mechanism leading to green-tides. Estuar Coast Shelf Sci 227:106329

  60. Xu D, Gao Z, Zhang X, Qi Z, Meng C, Zhuang Z, Ye N (2011) Evaluation of the potential role of the macroalga Laminaria japonica for alleviating coastal eutrophication. Bioresour Technol 102:9912–9918

  61. Ye N, Zhang X, Mao Y, Liang C, Xu D, Zou J, Zhuang Z, Wang Q (2011) ‘Green tides’ are overwhelming the coastline of our blue planet: taking the world’s largest example. Ecol Res 26:477–485

  62. Yuan L, Loque D, Ye F, Frommer WB, von Wiren N (2007) Nitrogen-dependent posttranscriptional regulation of the ammonium transporter AtAMT1;1. Plant Physiol 143:732–744

  63. Zhang X, Xu D, Mao Y, Li Y, Xue S, Zou J, Lian W, Liang C, Zhuang Z, Wang Q (2011) Settlement of vegetative fragments of Ulva prolifera confirmed as an important seed source for succession of a large-scale green tide bloom. Limnol Oceanogr 56:233–242

Download references

Funding

This work was supported by National Key Research and Development Program of China (2018YFD0900705, 2018YFD0900703, 2018YFD0901503, 2016YFC1402102); National Natural Science Foundation of China (41976110, 41676145); Shandong key Research and Development Plan (2018GHY115010); Special Scientific Research Funds for Central Non-Profit Institutes, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences (20603022019006, 20603022016001); Youth Talent Program Supported by Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao) (2018-MFS-01); China Agriculture Research System (CARS-50); Marine S&T Fund of Shandong Province for Pilot National Laboratory for Marine Science and Technology (Qingdao) (No. 2018SDKJ0406-3); Financial Fund of the Ministry of Agriculture and Rural Affairs, P. R. of China (NFZX2018); Taishan Scholars Funding; Talent Projects of Distinguished Scientific Scholars in Agriculture; Shandong Provincial Natural Science Foundation, China (ZR2017MD025).

Author information

Correspondence to Naihao Ye.

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 3.29 MB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Fan, X., Xu, D., Wang, D. et al. Nutrient uptake and transporter gene expression of ammonium, nitrate, and phosphorus in Ulva linza: adaption to variable concentrations and temperatures. J Appl Phycol (2020). https://doi.org/10.1007/s10811-020-02050-2

Download citation

Keywords

  • Nutrient uptake rate (NUR)
  • Nutrient transporter gene expression
  • Concentration
  • Temperature
  • Chlorophyceae
  • Ulva linza