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Nitrogen uptake and growth responses of seedlings of the brown seaweed Sargassum hemiphyllum under controlled culture conditions

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Abstract

For the purpose of indoor mass culture of seedlings of Sargassum hemiphyllum during spring and summer, a series of experiments were designed to evaluate nitrogen (N) uptake, growth performance, and N accumulation of seedlings. Transient uptake rates by N-limited seedlings for nitrate (NO3 −), ammonium (NH4 +), and urea were more rapid than uptake rates by N-replete seedlings. NO3 − uptake revealed a rate-saturating uptake kinetic for both N-limited and N-replete seedlings. Uptake rates of NH4 + and urea for N-limited seedlings were linear, whereas the N-replete seedlings displayed Michaelis-Menten curves. The slope of the linear models or equivalently affinity calculated from Michaelis-Menten curves was highest for NH4 + and lowest for urea, indicating that seedlings were more efficient at taking up NH4 +. Tissue N content in seedling increased with increasing N concentrations, with the highest values with all three N sources at 150 μM. The N requirement to support maximum growth varied 2.2-fold from 0.39 ± 0.15% dry weight (DW) in NH4 + to 0.84 ± 0.09% DW in NO3 −, and hence, seedlings became more easily N limited at low NO3 − availability. The results showed that seedlings cultured in NO3 − enrichment (50–100 μM) may be better able to meet their maximum growth than at high NH4 + availability, although seedlings have higher NH4 + uptake capacities.

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References

  • Abreu MH, Pereira R, Buschmann AH, Sousa-Pinto I, Yarish C (2011) Nitrogen uptake responses of Gracilaria vermiculophylla (Ohmi) Papenfuss under combined and single addition of nitrate and ammonium. J Exp Mar Biol Ecol 407:190–199

    Article  CAS  Google Scholar 

  • Ahn O, Petrell RJ, Harrison PJ (1998) Ammonium and nitrate uptake by Laminaria saccharina and Nereocystis luetkeana originating from a salmon sea cage farm. J Appl Phycol 10:333–340

    Article  CAS  Google Scholar 

  • Braga AC, Yoneshigue-Valentin Y (1996) Nitrogen and phosphorus uptake by the Brazilian kelp Laminaria abyssalis (Phaeophyta) in culture. Hydrobiologia 326/327:445–450

    Article  Google Scholar 

  • Cochlan WP, Harrison PJ (1991) Kinetics of nitrogen (nitrate, ammonium, urea) uptake by the picoflagellate Micromonas pusilla (Prasinophyceae). J Exp Mar Biol Ecol 153:129–141

    Article  CAS  Google Scholar 

  • D’Elia CF, DeBoer JA (1978) Nutritional studies of two red algae: II. Kinetics of ammonium and nitrogen uptake. J Phycol 14:266–272

    Article  Google Scholar 

  • Droop MR (1983) 25 years of algal growth kinetics: a personal view. Bot Mar 26:99–112

    Article  Google Scholar 

  • Fong P, Fong JJ, Fong CR (2004) Growth, nutrient storage, and release of dissolved organic nitrogen by Enteromorpha intestinalis in response to pulses of nitrogen and phosphorus. Aquat Bot 78:83–95

    Article  CAS  Google Scholar 

  • Fujita RM (1985) The role of nitrogen status in regulating transient ammonium uptake and nitrogen storage by macroalgae. J Exp Mar Biol Ecol 92:283–301

    Article  CAS  Google Scholar 

  • Fujita RM, Wheeler PA, Edwards RL (1988) Metabolic regulation of ammonium uptake by Ulva rigida (Chlorophyta): a compartmental analysis of the rate-limiting step for uptake. J Phycol 24:560–566

    Article  CAS  Google Scholar 

  • Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 29–60

    Chapter  Google Scholar 

  • Hanisak MD (1983) The nitrogen relationships of marine macroalgae. In: Carpenter EJ, Capone DG (eds) Nitrogen in the marine environment. Academic, New York, pp 699–730

    Chapter  Google Scholar 

  • Harrison PJ, Hurd CL (2001) Nutrient physiology of seaweeds: application of concepts to aquaculture. Cah Biol Mar 42:71–82

    Google Scholar 

  • Harrison PJ, Parslow JS, Conway HL (1989) Determination of nutrient uptake kinetic parameters: a comparison of methods. Mar Ecol Prog Ser 52:301–312

    Article  Google Scholar 

  • Healey FP (1980) Slope of the Monod equation as an indicator of advantage in nutrient competition. Microb Ecol 5:281–286

    Article  CAS  PubMed  Google Scholar 

  • Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology. Cambridge University Press, New York, pp 244–263

    Book  Google Scholar 

  • Jia C, Yang B, Xie EY (2012) Studies on the prevention and cure for predators and rivals in artificial breeding of Sargassum naozhouense Tseng et Lu. J Aquac 33(7):35–39 (in Chinese with English abstract)

    Google Scholar 

  • Kang YH, Park SR, Chung IK (2011) Biofiltration efficiency and biochemical composition of three seaweed species cultivated in a fish-seaweed integrated culture. Algae 26:97–108

    Article  Google Scholar 

  • Kraemer GP, Carmona R, Chopin T, Neefus C, Tang X, Yarish C (2004) Evaluation of the bioremediatory potential of several species of the red alga Porphyra using short-term measurements of nitrogen uptake as a rapid bioassay. J Appl Phycol 16:489–497

    Article  CAS  Google Scholar 

  • Liu HX, Huang LM, Song XY, Zhong Y (2012) Using primary productivity as an index of coastal eutrophication: a case study in Daya Bay. Water Environ J 26:235–240

    Article  CAS  Google Scholar 

  • Liu F, Pang SJ, Gao SQ (2016) Growth performance of unialgal gametophytes of the brown alga Saccharina japonica in mass culture conditions. J Appl Phycol 28:1145–1152

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Martínez B, Rico JM (2004) Inorganic nitrogen and phosphorus uptake kinetics in Palmaria palmata (Rhodophyta). J Phycol 40:642–650

    Article  Google Scholar 

  • Martínez B, Pato LS, Rico JM (2012) Nutrient uptake and growth responses of three intertidal macroalgae with perennial, opportunistic and summer-annual strategies. Aquat Bot 96:14–22

    Article  Google Scholar 

  • Mengel K (1992) Nitrogen: agricultural productivity and environmental problems. In: Mengel K, Pilbeam DL (eds) Nitrogen Metabolism of Plants. Clarendon Press, Oxford, pp 1–15

    Google Scholar 

  • Morgan KC, Simpson FJ (1981) Cultivation of Palmaria (Rhodymenia) palmata: effect of high concentrations of nitrate and ammonium on growth and nitrogen uptake. Aquat Bot 11:167–171

    Article  CAS  Google Scholar 

  • O’Brien MC, Wheeler PA (1987) Short term uptake of nutrients by Enteromorpha prolifera (Chlorophyta). J Phycol 23:547–556

    Article  Google Scholar 

  • Ohno M, Arai S, Watanabe M (1990) Seaweed succession on artificial reefs on different substrata. J Appl Phycol 2:323–332

    Article  Google Scholar 

  • Pedersen MF (1994) Transient ammonium uptake in the macroalga Ulva lactuca (Chlorophyta): nature, regulation, and the consequences for the choice of measuring technique. J Phycol 30:980–986

    Article  Google Scholar 

  • Pedersen MF, Borum J (1996) Nutrient control of alga growth in estuarine waters. Nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macroalgae. Mar Ecol Prog Ser 142:261–272

    Article  CAS  Google Scholar 

  • Pedersen MF, Borum J (1997) Nutrient control of estuarine macroalgae: growth strategy and the balance between nitrogen requirements and uptake. Mar Ecol Prog Ser 161:155–163

    Article  Google Scholar 

  • Pedersen MF, Borum J, Fotel FL (2010) Phosphorus dynamics and limitation of fast- and slow-growing temperate seaweeds in Oslofjord, Norway. Mar Ecol Prog Ser 399:103–115

    Article  CAS  Google Scholar 

  • Pereira R, Kraemer G, Yarish C, Sousa-pinto I (2008) Nitrogen uptake by gametophytes of Porphyra dioica (Bangiales, Rhodophyta) under controlled-culture conditions. Eur J Phycol 43:107–118

    Article  CAS  Google Scholar 

  • Phillips JC, Hurd CL (2003) Nitrogen ecophysiology of intertidal seaweeds from New Zealand: N uptake, storage and utilization in relation to shore position and season. Mar Ecol Prog Ser 264:31–48

    Article  Google Scholar 

  • Phillips JC, Hurd CL (2004) Kinetics of nitrate, ammonium, and urea uptake by four intertidal seaweeds from New Zealand. J Phycol 40:534–545

    Article  CAS  Google Scholar 

  • Randall DJ, Tsui TKN (2002) Ammonia toxicity in fish. Mar Pollut Bull 45:17–23

    Article  CAS  PubMed  Google Scholar 

  • Revilla M, Alexander J, Glibert PM (2005) Urea analysis in coastal waters: comparison of enzymatic and direct methods. Limnol Oceanogr Methods 3:290–299

    Article  CAS  Google Scholar 

  • Rosenberg G, Ramus J (1982) Ecological growth strategies in the seaweeds Gracilaria foliifera (Rhodophyceae) and Ulva sp. (Chlorophyceae): soluble nitrogen and reserve carbohydrates. Mar Biol 66:251–259

    Article  Google Scholar 

  • Smit AJ (2002) Nitrogen uptake by Gracilaria gracilis (Rhodophyta): adaptations to a temporally variable nitrogen environment. Bot Mar 45:196–209

    Article  CAS  Google Scholar 

  • Smit AJ, Robertson BL, du Preez DR (1997) Influence of ammonium-N pulse concentrations and frequency, tank condition and nitrogen starvation on growth rate and biochemical composition of Gracilaria gracilis. J Appl Phycol 8:473–481

    Article  Google Scholar 

  • Terawaki T, Yoshikawa K, Yoshida G, Uchimura M, Iseki K (2003) Ecology and restoration techniques for Sargassum beds in the Seto Inland Sea. Jpn Mar Poll Bull 47:198–201

    Article  CAS  Google Scholar 

  • Wang C, Lei AP, Zhou K, Hu ZY, Hao WL, Yang JD (2014a) Growth and nitrogen uptake characteristics reveal outbreak mechanism of the opportunistic macroalga Gracilaria tenuistipitata. PLoS One 9:e108980

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang ZH, Song SH, Qi YZ (2014b) A comparative study of phytoneuston and the phytoplankton community structure in Daya Bay, South China Sea. J Sea Res 85:474–482

    Article  Google Scholar 

  • Wilson KL, Kay LM, Schmidt AL, Lotze HK (2015) Effects of increasing water temperatures on survival and growth of ecologically and economically important seaweeds in Atlantic Canada: implications for climate change. Mar Biol 162:2431–2444

    Article  CAS  Google Scholar 

  • Wu ML, Wang YS, Gu JD (2015) Assessment for water quality by artificial neural network in Daya Bay, South China Sea. Ecotoxicology 24:1632–1642

    Article  CAS  PubMed  Google Scholar 

  • Xie EY, Liu DC, Jia C, Chen XL, Yang B (2013) Artificial seed production and cultivation of the edible brown alga Sargassum naozhouense Tseng et Lu. J Appl Phycol 25:513–522

    Article  Google Scholar 

  • Xu D, Gao ZQ, Zhang XW, Qi ZH, Meng CX, Zhuang ZM, Ye NH (2011) Evaluation of the potential role of the macroalga Laminaria japonica for alleviating coastal eutrophication. Bioresour Technol 102:9912–9918

    Article  CAS  PubMed  Google Scholar 

  • Yoon JT, Sun SM, Chu G (2014) Sargassum bed restoration by transplantation of germlings grown under protective mesh cage. J Appl Phycol 26:505–509

    Article  CAS  Google Scholar 

  • Yu YQ, Zhang QS, Tang YZ, Zhang SB, Lu ZC, Chu SH, Tang XX (2012) Establishment of intertidal seaweed beds of Sargassum thunbergii through habit creation and germling seeding. Ecol Eng 44:10–17

    Article  Google Scholar 

  • Zhao SF, Ye TL, Sun HQ (2013) Clearing Bryopsis caespitosa off Sargassum leizhouense germlings by ecological method under laboratory conditions. J Aquac 34:37–41 (in Chinese with English abstract)

    Google Scholar 

Download references

Acknowledgements

This study was supported by Special Fund of Basic Research for Central Non-Profit Scientific Research Institutes (2014A01YY03), National Natural Science Foundation of China (31602183), Guangdong Natural Science Foundation (2014A030310331), Major State Basic Research Development Program of China (973 Program, 2015CB452901, 2015CB4529004), the Key Laboratory of South China Sea Fishery Resources Development and Utilization, Ministry of Agriculture (LSF2014-05), Pear River S&T Nova Program of Guangzhou (2013J2200092), and Project of Science and Technology of Guangdong Province (2013B020503053).

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Authors and Affiliations

  1. Guangdong Provincial Key Laboratory of Fishery Ecology Environment and Key Laboratory of South China Sea Fishery Resources Exploitation and Utilization, Ministry of Agriculture, South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, 231 Xingangxi Road, Guangzhou, 510300, People’s Republic of China

    Tingting Han, Zhanhui Qi, Honghui Huang, Xiuli Liao & Wenwen Zhang

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  1. Tingting Han
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Correspondence to Honghui Huang.

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Han, T., Qi, Z., Huang, H. et al. Nitrogen uptake and growth responses of seedlings of the brown seaweed Sargassum hemiphyllum under controlled culture conditions. J Appl Phycol 30, 507–515 (2018). https://doi.org/10.1007/s10811-017-1216-1

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  • DOI: https://doi.org/10.1007/s10811-017-1216-1

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