Skip to main content

Advertisement

SpringerLink
Log in

Effects of high ammonium level on biomass accumulation of common duckweed Lemna minor L.

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Growing common duckweed Lemna minor L. in diluted livestock wastewater is an alternative option for pollutants removal and consequently the accumulated duckweed biomass can be used for bioenergy production. However, the biomass accumulation can be inhibited by high level of ammonium (NH4 +) in non-diluted livestock wastewater and the mechanism of ammonium inhibition is not fully understood. In this study, the effect of high concentration of NH4 + on L. minor biomass accumulation was investigated using NH4 + as sole source of nitrogen (N). NH4 +-induced toxicity symptoms were observed when L. minor was exposed to high concentrations of ammonium nitrogen (NH4 +-N) after a 7-day cultivation. L. minor exposed to the NH4 +-N concentration of 840 mg l−1 exhibited reduced relative growth rate, contents of carbon (C) and photosynthetic pigments, and C/N ratio. Ammonium irons were inhibitory to the synthesis of photosynthetic pigments and caused C/N imbalance in L. minor. These symptoms could further cause premature senescence of the fronds, and restrain their reproduction, growth and biomass accumulation. L. minor could grow at NH4 +-N concentrations of 7–84 mg l−1 and the optimal NH4 +-N concentration was 28 mg l−1.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  • Ariz I, Asensio AC, Zamarreño AM, García-Mina JM, Aparicio-Tejo PM, Moran JF (2013) Changes in the C/N balance caused by increasing external ammonium concentrations are driven by carbon and energy availabilities during ammonium nutrition in pea plants: the key roles of asparagine synthetase and anaplerotic enzymes. Physiol Plant 148:522–537

    Article  CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  Google Scholar 

  • Baliban RC, Elia JA, Floudas CA, Xiao X, Zhang Z, Li J, Cao H, Ma J, Qiao Y, Hu X (2013) Thermochemical conversion of duckweed biomass to gasoline, diesel, and jet fuel: process synthesis and global optimization. Ind Eng Chem Res 52:11436–11450

    Article  CAS  Google Scholar 

  • Boussadia O, Steppe K, Zgallai H, Ben El Hadj S, Braham M, Lemeur R, van Labekee MC (2010) Effects of nitrogen deficiency on leaf photosynthesis, carbohydrate status and biomass production in two olive cultivars ‘Meski’ and ‘Koroneiki’. Sci Hortic 123:336–342

    Article  CAS  Google Scholar 

  • Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159:567–584

    Article  CAS  Google Scholar 

  • Caicedo JR, van der Steennp NP, Arce O, Gijzen HJ (2000) Effect of total ammonia nitrogen concentration and pH on growth rates of duckweed (Spirodela polyrrhiza). Water Res 34:3829–3835

    Article  CAS  Google Scholar 

  • Cao T, Ni LY, Xie P (2004) Acute biochemical responses of a submersed macrophyte, Potamogeton crispus L, to high ammonium in an aquarium experiment. J Freshw Ecol 19:279–284

    Article  CAS  Google Scholar 

  • Cedergreen N, Madsen TV (2002) Nitrogen uptake by the floating macrophyte Lemna minor. New Phytol 155:285–292

    Article  Google Scholar 

  • Cheng LJ, Cheng TS (2012) Oxidative effects and metabolic changes following exposure of greater duckweed (Spirodela polyrhiza) to diethyl phthalate. Aquat Toxicol 109:166–175

    Article  CAS  Google Scholar 

  • Cheng JJ, Stomp AM (2009) Growing duckweed to recover nutrients from wastewaters and for production of fuel ethanol and animal feed. Clean Soil Air Water 37:17–26

    Article  CAS  Google Scholar 

  • Cheng J, Landesman L, Bergmann BA, Classen JJ, Howard JW, Yamamoto YT (2002) Nutrient removal from swine lagoon liquid by Lemna minor 8627. Trans ASAE 45:1003–1010

    Google Scholar 

  • Clement B, Bouvet Y (1993) Assessment of landfill leachate toxicity using the duckweed Lemna minor. Sci Total Environ 41:1179–1190

    Article  Google Scholar 

  • Coskun D, Britto DT, Li M, Becker A, Kronzucker HJ (2013) Rapid ammonia gas transport accounts for futile transmembrane cycling under NH3/NH4 + toxicity in plant roots. Plant Physiol 163:1859–1867

    Article  CAS  Google Scholar 

  • Dordio A, Carvalho AJP (2013) Constructed wetlands with light expanded clay aggregates for agricultural wastewater treatment. Sci Total Environ 463–464:454–461

    Article  Google Scholar 

  • Duan PG, Xu YP, Bai XJ (2013) Upgrading of crude duckweed bio-oil in subcritical water. Energy Fuel 27:4729–4738

    Article  CAS  Google Scholar 

  • Fang YY, Babourina O, Rengel Z, Yang XE, Pu PM (2007) Ammonium and nitrate uptake by the floating plant Landoltia punctata. Ann Bot 99:365–370

    Article  CAS  Google Scholar 

  • Fedler CB, Duan RB (2011) Biomass production for bioenergy using recycled wastewater in a natural waste treatment system. Resour Conserv Recycl 55:793–800

    Article  Google Scholar 

  • Ge XM, Zhang NN, Phillips GC, Xu JF (2012) Growing Lemna minor in agricultural wastewater and converting the duckweed biomass to ethanol. Bioresour Technol 124:485–488

    Article  CAS  Google Scholar 

  • Goopy JP, Murray PJ (2003) A review on the role of duckweed in nutrient reclamation and as a source of animal feed. Asian Aust J Anim Sci 16:297–305

    Google Scholar 

  • Huang L, Lu YY, Gao X, Du G, Ma X, Liu M, Guo J, Chen Y (2013) Ammonium-induced oxidative stress on plant growth and antioxidative response of duckweed (Lemna minor L.). Ecol Eng 58:355–362

    Article  Google Scholar 

  • ISO (2006) Determination of the toxic effect of water constituents and wastewater on duckweed (Lemna minor)—duckweed growth inhibition test. ISO norm 20079

  • Jampeetong A, Brix H (2009) Effects of NH4 + concentration on growth, morphology and NH4 + uptake kinetics of Salvinia natans. Ecol Eng 35:695–702

    Article  Google Scholar 

  • Kopsell DA, Kopsell DE, Curran-Celentano J (2007) Carotenoid pigments in kale are influenced by nitrogen concentration and form. J Sci Food Agric 87:900–907

    Article  CAS  Google Scholar 

  • Kosová K, Vítámvás P, Prášil IT, Renaut J (2012) Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. Plant Signal Behav 7:1456–1466

    Article  Google Scholar 

  • Leng RA, Stambolie JH, Bell R (1995) Duckweed—a potential high-protein feed resource for domestic animals and fish. Livest Res Rural Dev 7:1–12

    Google Scholar 

  • Li B, Li G, Kronzucker HJ, Baluška F, Shi W (2013) Ammonium stress in Arabidopsis: signaling, genetic loci, and physiological targets. Trends Plant Sci S1:360–1385

    Article  Google Scholar 

  • Logan BA, Demmig-Adams B, Rosenstiel TH, Adams WW (1999) Effect of nitrogen limitation on foliar antioxidants in relationship to other metabolic characteristics. Planta 209:213–220

    Article  CAS  Google Scholar 

  • Mohedano RA, Costa RHR, Tavares FA, Filho PB (2012) High nutrient removal rate from swine wastes and protein biomass production by full-scale duckweed ponds. Bioresour Technol 112:98–104

    Article  CAS  Google Scholar 

  • Olguin EJ, Sanchez-Galvan G, Perez-Perez T (2007) Assessment of the phytoremediation potential of Salvinia minima baker compared to Spirodela polyrrhiza in high-strength organic wastewater. Water Air Soil Pollut 181:135–147

    Article  CAS  Google Scholar 

  • Porath D, Pollock J (1982) Ammonia stripping by duckweed and its feasibility in circulating aquaculture. Aquat Bot 13:125–131

    Article  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Priya A, Avishek K, Pathak G (2012) Assessing the potentials of Lemna minor in the treatment of domestic wastewater at pilot scale. Environ Monit Assess 184:4301–4307

    Article  CAS  Google Scholar 

  • Radić S, Pevalek-Kozlina B (2010) Effects of osmotic stress on antioxidative system of duckweed (Lemna minor L). Period Biol 112:293–299

    Google Scholar 

  • Radić S, Stipaničev D, Cvjetko P, Marijanović Rajčić M, Sirac S, Pevalek-Kozlina B, Pavlica M (2011) Duckweed Lemna minor as a tool for testing toxicity and genotoxicity of surface waters. Ecotoxicol Environ Saf 74:182–187

    Article  Google Scholar 

  • Rudolph H, Voigt JU (1986) Effects of NH4 +-N and NO3 –-N on growth and metabolism of Sphagnum magellanicum. Physiol Plant 66:339–343

    Article  Google Scholar 

  • Sims A, Gajaraj S, Hu Z (2013) Nutrient removal and greenhouse gas emissions in duckweed treatment ponds. Water Res 47:1390–1398

    Article  CAS  Google Scholar 

  • Stevens CJ, Manning P, van den Berg LJL, de Graaf MCC, Wamelink GWW, Boxman AW, Bleeker A, Vergeer P, Arroniz-Crespo M, Limpens J, Lamers LPM, Bobbink R, Dorland E (2011) Ecosystem responses to reduced and oxidised nitrogen inputs in European terrestrial habitats. Environ Pollut 159:665–676

    Article  CAS  Google Scholar 

  • van Breemen N, Burrough PA, Velthorst EJ, van Dobben HF, de Wit T, Ridder TB, Reijnders HF (1982) Soil acidification from atmospheric ammonium sulphate in forest canopy throughfall. Nature 299:548–550

    Article  Google Scholar 

  • van Katwijk MM, Vergeer LHT, Schmitz GHW, Roelofs JGM (1997)Ammonium toxicity in eelgrass Zostera marina. Mar Ecol Prog Ser 157:159–173

    Article  Google Scholar 

  • von Wirén N, Gazzarrini S, Gojon A, Frommer WB (2000) The molecular physiology of ammonium uptake and retrieval. Curr Opin Plant Biol 3:254–261

    Article  Google Scholar 

  • Wang C, Zhang SH, Li W, Wang PF, Li L (2011) Nitric oxide supplementation alleviates ammonium toxicity in the submerged macrophyte Hydrilla verticillata (L.f.) Royle. Ecotoxicol Environ Saf 74:67–73

    Article  CAS  Google Scholar 

  • Wangermann E, Ashby E (1950) A discussion on morphogenesis: morphogenesis in Lemna minor. Proc Linn Soc Lond 162:10–13

    Article  Google Scholar 

  • Xiao Y, Fang Y, Jin YL, Zhang GH, Zhao H (2013) Culturing duckweed in the field for starch accumulation. Ind Crop Prod 48:183–190

    Article  CAS  Google Scholar 

  • Xu J, Shen G (2011) Growing duckweed in swine wastewater for nutrient recovery and biomass production. Bioresour Technol 102:848–853

    Article  CAS  Google Scholar 

  • Zhang M, Wang Z, Xu J, Liu Y, Ni L, Cao T, Xie P (2011) Ammonium, microcystins, and hypoxia of blooms in eutrophic water cause oxidative stress and C–N imbalance in submersed and floating-leaved aquatic plants in Lake Taihu, China. Chemosphere 82:329–339

    Article  CAS  Google Scholar 

  • Zheng ZL (2009) Carbon and nitrogen nutrient balance signaling in plants. Plant Signal Behav 4:584–591

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the NSFC project (51108239) and Applied Basic Research Program of Sichuan Province (2013JY0005).

Author information

Authors and Affiliations

  1. Biogas Institute of Ministry of Agriculture, Chengdu, 610041, China

    Wenguo Wang, Xiaoyu Tang, Xinjiao Gu, Qili Zhu, Ke Pan & Qichun Hu

  2. College of Life Sciences, Sichuan Normal University, Chengdu, 610061, China

    Chuang Yang & Danwei Ma

Authors
  1. Wenguo Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chuang Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaoyu Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xinjiao Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qili Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ke Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qichun Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Danwei Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wenguo Wang.

Additional information

Responsible editor: Elena Maestri

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, W., Yang, C., Tang, X. et al. Effects of high ammonium level on biomass accumulation of common duckweed Lemna minor L.. Environ Sci Pollut Res 21, 14202–14210 (2014). https://doi.org/10.1007/s11356-014-3353-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3353-2

Keywords

Search

Navigation