Environmental Science and Pollution Research

, Volume 26, Issue 1, pp 775–783 | Cite as

The remediation potential and kinetics of cadmium in the green alga Cladophora rupestris

  • Hui-min Zhang
  • Geng Geng
  • Jun-jie Wang
  • Yue Xin
  • Qian Zhang
  • De-ju CaoEmail author
  • You-hua Ma
Research Article


This study determined the subcellular distribution, chemical forms, and effects of metal homeostasis of excess Cd in Cladophora rupestris. Biosorption data were analyzed with Langmuir and Freundlich adsorption models and kinetic equations. Results showed that C. rupestris can accumulate Cd. Cd mainly localized in the cell wall and debris (42.8–68.2%) of C. rupestris, followed by the soluble fraction (22.1–38.4%) observed in C. rupestris. A large quantity of Cd ions existed as insoluble CdHPO4 complexed with organic acids, Cd(H2PO4)2, Cd-phosphate complexes (FHAC) (43.2–56.0%), and pectate and protein-integrated Cd (FNaCl) (30.8–43.2%). The adsorption data were well fitted by the Freundlich model (R2 = 0.933) and could be described by the pseudo-second-order reaction rate (R2 = 0.997) and Elovich (R2 = 0.972) equations. Related parameters indicated that Cd adsorption by C. rupestris is a heterogeneous diffusion. Cd promoted Ca and Zn uptake by C. rupestris. Cu, Fe, Mn, and Mg adsorption was promoted by low Cd concentrations and inhibited by high Cd concentrations. Results suggested that cell wall sequestration, vacuolar compartmentalization, and chemical morphological transformation are important mechanisms of Cd stress tolerance by C. rupestris. This study suggests that C. rupestris has bioremediation potential of Cd.


Cd C. rupestris Kinetics Bioaccumulation Subcellular distribution Chemical form 


Funding information

This work was under the financial aid of the Natural Science Foundation of China (41877418), Nature Fund of Anhui Province of China (1808085MD100), and the Key S&T Special Projects of Anhui Province of China (17030701053), and funding for this study was also provided by the Natural Students’ Innovation and Entrepreneurship Training Program (201710364058).


  1. Anastopoulos I, Kyzas GZ (2015) Progress in batch biosorption of heavy metals onto algae. J Mol Liq 209:77–86CrossRefGoogle Scholar
  2. Areco MM, Hanela S, Duran J, Afonso MS (2012) Biosorption of Cu(II), Zn(II), Cd(II) and Pb(II) by dead biomasses of green alga Ulva lactuca and the development of a sustainable matrix for adsorption implementation. J Hazard Mater 213–214:123–132CrossRefGoogle Scholar
  3. ATDR (2012) Toxicological profile for cadmium, Agency for Toxic Substances and Disease Registry. Public Health Services, US Department of Health and Human Services. J Mol Liq 209:77–86Google Scholar
  4. Bai X, Chen YH, Geng K et al (2014) Accumulation, subcellular distribution and chemical forms of cadmium in Viola tricolor L. China. J Acta Scientiae Circumstantiae 34(6):1600–1605Google Scholar
  5. Brooks RR, Lee J, Reeves RD, Jaffre T (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–77CrossRefGoogle Scholar
  6. Brune A, Urbach W, Detz KJ (2008) Compartmentation and transport of zinc in barley primary leaves as basic mechanism involved in zinc tolerance. Plant Cell Environ 17:153–162CrossRefGoogle Scholar
  7. Cao DJ, Shi XD, Li H, Xie PP, Zhang HM, Deng JW, Liang YG (2015a) Effects of lead on tolerance, bioaccumulation, and antioxidative defense system of green algae, Cladophora. Ecotoxicol Environ Saf 112:231–237CrossRefGoogle Scholar
  8. Cao DJ, Xie PP, Deng JW, Zhang HM, Ma RX, Liu C, Liu RJ, Liang YG, Li H, Shi XD (2015b) Effects of Cu2+ and Zn2+ on growth and physiological characteristics of green algae, Cladophora. Environ Sci Pollut Res 22:16535–16541CrossRefGoogle Scholar
  9. Cao DJ, Yang X, Geng G, Wan XC, Ma RX, Zhang Q, Liang YG (2018) Absorption and subcellular distribution of cadmium in tea plant (Camellia sinensis cv. “Shuchazao”). Environ Sci Pollut Res 25(16):15357–15367CrossRefGoogle Scholar
  10. Chakravarty R, Banerjee PC (2012) Mechanism of cadmium binding on the cell wall of an acidophilic bacterium. Bioresour Technol 108:176–183CrossRefGoogle Scholar
  11. Ding Y, Liu Y, Liu S, Li Z, Tan X, Huang X, Zeng G, Zhou Y, Zheng B, Cai X (2016) Competitive removal of Cd(II) and Pb(II) by biochars produced from water hyacinths: performance and mechanism. RSC Adv 6:5223–5232CrossRefGoogle Scholar
  12. Doshi H, Ray A, Kothari IL (2007) Bioremediation potential of live and dead Spirulina: spectroscopic, kinetics and SEM studies. Biotechnol Bioeng 96:1051–1063CrossRefGoogle Scholar
  13. Fan JL, Zhang J, Zhang CL et al (2011) Adsorption of 2,4,6-trichlorophenol from aqueous solution onto activated carbon derived from loosestrife. Desalination 267:139–146CrossRefGoogle Scholar
  14. Farhan AM, Al-Dujaili AH, Awwad AM (2013) Equilibrium and kinetic studies of cadmium(II) and lead(II) ions biosorption onto Ficus carcia leaves. Int J Ind Chem 4:24CrossRefGoogle Scholar
  15. Fu XP, Dou CM, Chen YX, Chen XC, Shi JY, Yu MG, Xu J (2011) Subcellular distribution and chemical forms of cadmium in Phytolacca americana L. J Hazard Mater 186:103–107CrossRefGoogle Scholar
  16. Hassler CS, Slaveykova VI, Wilkinson KJ (2004) Discrimination between intra- and extracellular metals using chemical extractions. Limnol Oceanogr Methods 2:237–247CrossRefGoogle Scholar
  17. Hernandez-Allica J, Garbisu C, Becerril JM et al (2006) Synthesis of low molecular weight thiols in response to Cd exposure in Thlaspi caerulescens. Plant Cell Environ 29(7):1422–1429CrossRefGoogle Scholar
  18. Hou M, Hu CJ, Xiong L, Lu C (2013) Tissue accumulation and subcellular distribution of vanadium in Brassica juncea and Brassica chinensis. Microchem J 110:575–578CrossRefGoogle Scholar
  19. Huang F, Dang Z, Guo CL, Lu GN, Gu RR, Liu HJ, Zhang H (2013) Biosorption of Cd(II) by live and dead cells of Bacillus cereus RC-1 isolated from cadmium-contaminated soil. Colloids Surf B 107:11–18CrossRefGoogle Scholar
  20. Islam MS, Saito T, Kurasaki M (2015) Phytofiltration of arsenic and cadmium by using an aquatic plant, Micranthemum umbrosum: phytotoxicity, uptake kinetics, and mechanism. Ecotoxicol Environ Saf 112:193–200CrossRefGoogle Scholar
  21. Kramer U, Pickering IJ, Prince RC et al (2000) Subcellular localization and speciation of nickel in hyperaccumulator and non-accumulator Thlaspi species. Physiol Plant 122:1343–1353CrossRefGoogle Scholar
  22. Krzesłowska M (2011) The cell wall in plant cell response to trace metals: polysaccharide remodeling and its role in defense strategy. Acta Physiol Plant 33:35–51CrossRefGoogle Scholar
  23. Kumar D, Pandey LK, Gaur JP (2016) Metal sorption by algal biomass: from batch to continuous system. Algal Res 18:95–109CrossRefGoogle Scholar
  24. Kupper H, Lombi E, Zhao FJ et al (2000) Cellular compartmentation of cadmium and zinc in relation to other elements in the hyperaccumulator Arabidopsis halleri. Planta 212(1):75–84CrossRefGoogle Scholar
  25. Lavoie M, Le Faucheur S, Fortin C, Campbell PGC (2009a) Cadmium detoxification strategies in two phytoplankton species: metal binding by newly synthesized thiolated peptides and metal sequestration in granules. Aquat Toxicol 92(2):65–75CrossRefGoogle Scholar
  26. Lavoie M, Bernier J, Fortin C, Campbell PGC (2009b) Cell homogenization and subcellular fractionation in two phytoplanktonic algae: implications for the assessment of metal subcellular distributions. Limnol Oceanogr Methods 7(4):277–286CrossRefGoogle Scholar
  27. Lavoie M, Fortin C, Campbell PGC (2012) Influence of essential elements on cadmium uptake and toxicity in a unicellular green alga: the protective effect of trace zinc and cobalt concentrations. Environ Toxicol Chem 31(7):1445–1452CrossRefGoogle Scholar
  28. Li H, Luo N, Zhang LJ, Zhao HM (2016) Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Sci Total Environ 571:1183–1190CrossRefGoogle Scholar
  29. Li XJ, Zheng XQ, Zheng SA (2017) Accumulation and sensitivity distribution of cadmium in leafy vegetables. J Res Environ Sci 30(5):720–727Google Scholar
  30. Lwalaba JLW, Zvobgo G, Mwamba M, Ahmed IM, Mukobo RPM, Zhang G (2017) Subcellular distribution and chemical forms of Co2+ in three barley genotypes under different Co2+ levels. Acta Physiol Plant 39:102CrossRefGoogle Scholar
  31. Ma J, Cai H, He C, Zhang W, Wang L (2015) A hemicellulose-bound form of silicon inhibits cadmium ion uptake in rice (Oryza sativa) cells. New Phytol 206:1063–1074CrossRefGoogle Scholar
  32. Mehta SK, Gaur JP (2001) Removal of Ni and Cu from single and binary metal solutions by free and immobilized Chlorella vulgaris. Eur J Protistol 271:261–271CrossRefGoogle Scholar
  33. Meyer CL, Juraniec M, Huguet S, Chaves-Rodriguez E, Salis P, Goormaghtigh E, Verbruggen N (2015) Intraspecific variability of cadmium tolerance and accumulation, and cadmium-induced cell wall modifications in the metal hyperaccumulator Arabidopsis halleri. J Exp Bot 66:3215–3217CrossRefGoogle Scholar
  34. Mwamba TM, Li L, Gill RA et al (2016) Differential subcellular distribution and chemical forms of cadmium and copper in Brassica napus. Ecotoxicol Environ Saf 134:239–249CrossRefGoogle Scholar
  35. Pillai SS, Mullassery MD, Fernandez NB, Girija N, Geetha P, Koshy M (2013) Biosorption of Cr(VI) from aqueous solution by chemically modified potato starch: equilibrium and kinetic studies. Ecotoxicol Environ Saf 92:199–205CrossRefGoogle Scholar
  36. Qiu Q, Wang Y, Yang Z, Yuan J (2011) Effects of phosphorus supplied in soil on subcellular distribution and chemical forms of cadmium in two Chinese flowering cabbage (Brassica parachinensis L) cultivars differing in cadmium accumulation. Food Chem Toxicol 49:2260–2267CrossRefGoogle Scholar
  37. Ren JT, Sheng L (2017) Regulation of calcium and magnesium homeostasis in plants: from transporters to signaling network. Curr Opin Plant Biol 39:97–105CrossRefGoogle Scholar
  38. Salt DE, Prince RC, Pickering IJ (2002) Chemical speciation of accumulated metals in plants: evidence from X-ray absorption spectroscopy. Microchem J 71:255–259CrossRefGoogle Scholar
  39. Sarret G, Harada E, Choi YE, Isaure MP, Geoffroy N, Fakra S, Marcus MA, Birschwilks M, Clemens S, Manceau A (2006) Trichomes of tobacco excrete zinc as zinc-substituted calcium carbonate and other zinc-containing compounds. Plant Physiol 141(3):1021–1034CrossRefGoogle Scholar
  40. Sarwar N, Malhi SS, Zia MH, Naeem A, Bibi S, Farid G (2010) Role of mineral nutrition in minimizing cadmium accumulation by plants. J Sci Food Agric 90:925–937Google Scholar
  41. Shen Y, Li H, Zhu WZ, Ho SH, Yuan WQ, Chen JF, Xie YP (2017) Microalgal-biochar immobilized complex: a novel efficient biosorbent for cadmium removal from aqueous solution. Bioresour Technol 244:1031–1038CrossRefGoogle Scholar
  42. Siedlecka A, Krupa Z (1999) Cd/Fe interaction in higher plants: its consequences for the photosynthetic apparatus. Photosynthetica 36:321–331CrossRefGoogle Scholar
  43. Singh A, Agrawal M, Marshall FM (2010) The role of organic vs. inorganic fertilizers in reducing phytoavailability of heavy metals in a wastewater-irrigated area. Ecol Eng 36:1733–1740CrossRefGoogle Scholar
  44. Talebi AF, Tabatabaei M, Mohtashami SK, Tohidfar M, Moradi F (2013) Comparative salt stress study on intracellular ion concentration in marine and salt-adapted freshwater strains of microalgae. Not Sci Biol 5(3):309–315CrossRefGoogle Scholar
  45. Wang L, Chen X, Wang H, Zhang Y, Tang Q, Li J (2017) Chlorella vulgaris cultivation in sludge extracts from 2,4,6-TCP wastewater treatment for toxicity removal and utilization. J Environ Manag 187:146–153CrossRefGoogle Scholar
  46. Xie PP, Deng JW, Zhang HM, Ma YH, Cao DJ, Ma RX, Liu RJ, Liu C, Liang YG (2015) Effects of cadmium on bioaccumulation and biochemical stress response in rice (Oryza sativa L). Ecotoxicol Environ Saf 122:392–398CrossRefGoogle Scholar
  47. Yang MQ, Li HY (2015) Study on biosorption of heavy metals by algae. Anhui Agricultural Sciences 43(28):257–259Google Scholar
  48. Zeraatkar AK, Ahmadzadeh H, Talebi AF, Moheimanic NR, McHenryd MP (2016) Potential use of algae for heavy metal bioremediation, a critical review. J Environ Manag 181:817–831CrossRefGoogle Scholar
  49. Zhang J, Tian SK, Lu LL et al (2011) Lead tolerance and cellular distribution in Elsholtzia splendens using synchrotron radiation micro-X-ray fluorescence. J Hazard Mater 197:264–271CrossRefGoogle Scholar
  50. Zhang HJ, Gao YT, Xiong HB (2017) Removal of heavy metals from polluted soil using the citric acid fermentation broth: a promising washing agent. Environ Sci Pollut Res 24:9506–9514CrossRefGoogle Scholar
  51. Zhao YF, Wu JF, Shang DR, Ning JS, Zhai YX, Sheng XF, Ding HY (2015) Subcellular distribution and chemical forms of cadmium in the edible seaweed, Porphyra yezoensis. Food Chem 168:48–54CrossRefGoogle Scholar
  52. Zhao S, Huang GH, Mu S, An CJ, Chen XJ (2017) Immobilization of phenanthrene onto gemini surfactant modified sepiolite at solid/aqueous interface: equilibrium, thermodynamic and kinetic studies. Sci Total Environ 598:619–627CrossRefGoogle Scholar
  53. Zhou XD, Li CY, Gao PX, Jiang XC, Zhao ZY, Han WS (2017) Adsorption of Cd2+ in water by living microalgae. Microbiol China 44(5):1182–1188Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Anhui Province Key Laboratory of Farmland Ecological Conservation and Pollution Prevention, School of Resources and EnvironmentAnhui Agricultural UniversityHefeiPeople’s Republic of China

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