Environmental Science and Pollution Research

, Volume 21, Issue 22, pp 12616–12628 | Cite as

Isotherm studies for the determination of Cd (II) ions removal capacity in living biomass of a microalga with high tolerance to cadmium toxicity

  • Enrique TorresEmail author
  • Roi Mera
  • Concepción Herrero
  • Julio Abalde
Research Article


The biosorption characteristics of Cd (II) ions using the living biomass of the marine diatom Phaeodactylum tricornutum were investigated. This microalga is a highly tolerant species to cadmium toxicity; for this reason, it is interesting to know its potential for use in the removal of this metal. The use of living biomass offers better possibilities than that of dead biomass since cadmium can also be bioaccumulated inside the cells. For this purpose, tolerant species are necessary. P. tricornutum is within this category with an EC50,96h of 19.1 ± 3.5 mg Cd (II)/L, and in the present manuscript, it is demonstrated that this microalga has a very good potential for bioremediation of Cd (II) ions in saline habitats. Cadmium removed by the cells was divided into three fractions: total, intracellular and bioadsorbed. The experiments were conducted for 96 h in natural seawater with a concentration range of 1–100 mg Cd (II)/L. Each fraction was characterized every 24 h by sorption isotherms. The experimental isotherm data were analyzed using the Langmuir, Freundlich, Dubinin-Radushkevich and Temkin equations. The biosorption was well described by Langmuir isotherm followed by Freundlich. The worst model was Temkin. The biosorption capacity of this microalga for Cd (II) ions was found to be 67.1 ± 3.2 mg/g after 96 h with approximately 40 % of this capacity in the intracellular fraction. The bioconcentration factor determined was 2,204.7 after 96 h and with an initial Cd (II) concentration of 1 mg/L.


Cadmium Biosorption isotherm Bioaccumulation Phaeodactylum tricornutum Living biomass 


  1. Abdel-Aty AM, Ammar NS, Abdel Ghafar HH, Ali RK (2013) Biosorption of cadmium and lead from aqueous solution by fresh water alga Anabaena sphaerica biomass. J Adv Res 4:367–374. doi: 10.1016/j.jare.2012.07.004
  2. Ahmady-Asbchin S, Tabaraki R, Jafari N, Allahverdi A, Azhdehakoshpour A (2013) Study of nickel and copper biosorption on brown algae Sargassum angustifolium: application of response surface methodology (RSM). Environ Technol 34:2423–2431CrossRefGoogle Scholar
  3. Aksu Z (2001) Equilibrium and kinetic modelling of cadmium(II) biosorption by C. vulgaris in a batch system: effect of temperature. Sep Pur Technol 21:285–294Google Scholar
  4. Bayramoĝlu G, Tüzün I, Çelik G, Yilmaz M, Arica MY (2006) Biosorption of mercury (II), cadmium (II) and lead (II) ions from aqueous system by microalgae Chlamydomonas reinhardtii immobilized in alginate beads. Int J Miner Process 81:35–43CrossRefGoogle Scholar
  5. Bering BP, Dubinin MN, Serpinsky VV (1972) On thermodynamics of adsorption in micropores. J Colloid Interface Sci 38:185–194CrossRefGoogle Scholar
  6. Chen CY, Chang HW, Kao PC, Pan JL, Chang JS (2012) Biosorption of cadmium by CO (2)-fixing microalga Scenedesmus obliquus CNW-N. Bioresour Technol 105:74–80. doi: 10.1016/j.biortech.2011.11.124 CrossRefGoogle Scholar
  7. Dixit S, Singh DP (2013) Phycoremediation of lead and cadmium by employing Nostoc muscorum as biosorbent and optimization of its biosorption potential. Int J Phytoremediation 15:801–813CrossRefGoogle Scholar
  8. Dönmez GÇ, Aksu Z, Öztürk A, Kutsal T (1999) A comparative study on heavy metal biosorption characteristics of some algae. Process Biochem 34:885–892CrossRefGoogle Scholar
  9. Doshi H, Ray A, Kothari IL (2007) Biosorption of cadmium by live and dead Spirulina: IR spectroscopic, kinetics and SEM studies. Curr Microbiol 54:213–218CrossRefGoogle Scholar
  10. Dubinin MM, Radushkevich LV (1947) Equation of characteristic curve of activated charcoal. Proc Acad Sci Phys Chem Sect USSR 55:331–333Google Scholar
  11. Folgar S, Torres E, Pérez-Rama M, Cid A, Herrero C, Abalde J (2009) Dunaliella salina as a marine microalga highly tolerant to but a poor remover of cadmium. J Hazard Mater 165:486–493. doi: 10.1016/j.jhazmat.2008.10.010 CrossRefGoogle Scholar
  12. Freundlich H (1906) Over the adsorption in solution. J Phys Chem 57:385Google Scholar
  13. Gaur N, Flora G, Yadav M, Tiwari A (2013) A review with recent advancements on bioremediation-based abolition of heavy metals. Environ Sci Process Impacts 15:180–193Google Scholar
  14. Gustafsson JP (2013) Visual MINTEQ version 3.1 [online]. Department of Land and Water Resources Engineering, Royal Institute of Technology, Stockholm, Sweden.Google Scholar
  15. Hall KR, Eagleton LC, Acrivos A, Vermeulen T (1966) Pore- and solid-diffusion kinetics in fixed-bed adsorption under constant-pattern conditions. Ind Eng Fund 5:212–223CrossRefGoogle Scholar
  16. Hasanuzzaman M, Fujita M (2013) Cadmium: characteristics, sources of exposure, health and environmental effects. In: Chemistry research and applications. Nova Publishers, New York, p 369Google Scholar
  17. Horvatić J, Peršić V (2007) The effect of Ni2+, Co2+, Zn2+, Cd2+ and Hg2+ on the growth rate of marine diatom Phaeodactylum tricornutum Bohlin: microplate growth inhibition test. Bull Environ Contam Toxicol 79:494–498. doi: 10.1007/s00128-007-9291-7 CrossRefGoogle Scholar
  18. Huang F, Dang Z, Guo C-L, Lu G-N, Gu RR, Liu H-J, Zhang H (2013) Biosorption of Cd(II) by live and dead cells of Bacillus cereus RC-1 isolated from cadmium-contaminated soil. Colloid Surface B 107:11–18. doi: 10.1016/j.colsurfb.2013.01.062
  19. Inthorn D, Sidtitoon N, Silapanuntakul S, Incharoensakdi A (2002) Sorption of mercury, cadmium and lead by microalgae. Sci Asia 28:253–261CrossRefGoogle Scholar
  20. Karnika AH, Reddy RS, Saradhi SV, Singh J (2007) An eco-friendly alternative for heavy metal removal. Afr J Biotechnol 6:2924–2931Google Scholar
  21. Katırcıo lu H, Aslım B, Rehber Türker A, Atici T, Beyatli Y (2008) Removal of cadmium (II) ion from aqueous system by dry biomass, immobilized live and heat-inactivated Oscillatoria sp. H1 isolated from freshwater (Mogan Lake). Bioresour Technol 99:4185–4191. doi: 10.1016/j.biortech.2007.08.068 CrossRefGoogle Scholar
  22. Kızılkaya B, Türker G, Akgül R, Doğan F (2011) Comparative study of biosorption of heavy metals using living green algae Scenedesmus quadricauda and Neochloris pseudoalveolaris: equilibrium and kinetics. J Dispers Sci Technol 33:410–419. doi: 10.1080/01932691.2011.567181 CrossRefGoogle Scholar
  23. Langmuir I (1918) The adsorption of gases on plane surfaces of glass, mica and platinum. J Am Chem Soc 40:1361–1403CrossRefGoogle Scholar
  24. Lezcano JM, Gonzalez F, Ballester A, Blazquez ML, Munoz JA, Garcia-Balboa C (2011) Sorption and desorption of Cd, Cu and Pb using biomass from an eutrophized habitat in monometallic and bimetallic systems. J Environ Manag 92:2666–2674. doi: 10.1016/j.jenvman.2011.06.004 CrossRefGoogle Scholar
  25. López-Chuken UJ, Young SD, Sánchez-González MN (2010) The use of chloro-complexation to enhance cadmium uptake by Zea mays and Brassica juncea: testing a “free ion activity model” and implications for phytoremediation. Int J Phytoremediation 12:680–696. doi: 10.1080/15226510903353161 CrossRefGoogle Scholar
  26. Lourie E, Gjengedal E (2011) Metal sorption by peat and algae treated peat: kinetics and factors affecting the process. Chemosphere 85:759–764. doi: 10.1016/j.chemosphere.2011.06.055 CrossRefGoogle Scholar
  27. Maret W, Moulis JM (2013) The bioinorganic chemistry of cadmium in the context of its toxicity. Met Ions Life Sci 11:1–29. doi: 10.1007/978-94-007-5179-8_1 CrossRefGoogle Scholar
  28. Matsunaga T, Takeyama H, Nakao T, Yamazawa A (1999) Screening of marine microalgae for bioremediation of cadmium-polluted seawater. J Biotechnol 70:33–38Google Scholar
  29. Michalak I, Chojnacka K, Witek-Krowiak A (2013) State of the art for the biosorption process—a review. Appl Biochem Biotechnol 170:1389–1416. doi: 10.1007/s12010-013-0269-0 CrossRefGoogle Scholar
  30. Millero FJ, Feistel R, Wright DG, McDougall TJ (2008) The composition of standard seawater and the definition of the reference-composition salinity scale. Deep-Sea Res PT I 55:50–72. doi: 10.1016/j.dsr.2007.10.001
  31. Monteiro CM, Brandao TR, Castro PM, Malcata FX (2012) Modelling growth of, and removal of Zn and Hg by a wild microalgal consortium. Appl Microbiol Biotechnol 94:91–100. doi: 10.1007/s00253-011-3826-x CrossRefGoogle Scholar
  32. Olguín EJ, Sánchez-Galván G (2012) Heavy metal removal in phytofiltration and phycoremediation: the need to differentiate between bioadsorption and bioaccumulation. New Biotechnol 30:3–8. doi: 10.1016/j.nbt.2012.05.020
  33. Pérez-Rama M, Torres E, Suárez C, Herrero C, Abalde J (2010) Sorption isotherm studies of Cd (II) ions using living cells of the marine microalga Tetraselmis suecica (Kylin) Butch. J Environ Manag 91:2045–2050. doi: 10.1016/j.jenvman.2010.05.014 CrossRefGoogle Scholar
  34. Rajamani S, Siripornadulsil S, Falcao V, Torres M, Colepicolo P, Sayre R (2007) Phycoremediation of heavy metals using transgenic microalgae. Adv Exp Med Biol 616:99–109. doi: 10.1007/978-0-387-75532-8_9 CrossRefGoogle Scholar
  35. Sarı A, Tuzen M (2008) Biosorption of cadmium (II) from aqueous solution by red algae (Ceramium virgatum): equilibrium, kinetic and thermodynamic studies. J Hazard Mater 157:448–454. doi: 10.1016/j.jhazmat.2008.01.008
  36. Sekabira K, Origa HO, Basamba TA, Mutumba G, Kakudidi E (2011) Application of algae in biomonitoring and phytoextraction of heavy metals contamination in urban stream water. Int J Environ Sci Technol 8:115–128. doi: 10.1007/BF03326201 CrossRefGoogle Scholar
  37. Singh SN, Tripathi RD (2007) Environmental bioremediation technologies. Springer, Berlin HeidelbergCrossRefGoogle Scholar
  38. Tangaromsuk J, Pokethitiyook P, Kruatrachue M, Upatham ES (2002) Cadmium biosorption by Sphingomonas paucimobilis biomass. Bioresour Technol 85:103–105CrossRefGoogle Scholar
  39. Temkin MJ, Pyzhev V (1940) Recent modifications to Langmuir isotherms. Acta Physiochim, URSS 12:217–222Google Scholar
  40. Torres E, Cid A, Fidalgo P, Herrero C, Abalde J (1995) Tolerance and detoxification mechanisms in marine diatom Phaeodactylum tricornutum exposed to cadmium. J Mar Biotechnol 3:176–178Google Scholar
  41. Torres E, Cid A, Fidalgo P, Herrero C, Abalde J (1997) Long-chain class III metallothioneins as a mechanism of cadmium tolerance in the marine diatom Phaeodactylum tricornutum Bohlin. Aquat Toxicol 39:231–246CrossRefGoogle Scholar
  42. Torres E, Cid A, Herrero C, Abalde J (1998) Removal of cadmium ions by the marine diatom Phaeodactylum tricornutum Bohlin accumulation and long-term kinetics of uptake. Bioresour Technol 63:213–220CrossRefGoogle Scholar
  43. Torres E, Mera R, Abalde J (2013) Toxicity and tolerance in microalgal cells exposed to cadmium: a current overview. In: Hasanuzzaman M, Fujita M (eds) Cadmium: characteristics, sources of exposure, health and environmental effects. Chemistry research and applications. Nova Publishers, New York, pp 171–196Google Scholar
  44. Tüzün I, Bayramoĝlu G, Yalçin E, Başaran G, Çelik G, Arica Y (2005) Equilibrium and kinetic studies on biosorption of Hg (II), Cd (II) and Pb (II) ions onto microalgae Chlamydomonas reinhardtii. J Environ Manage 77:85–92Google Scholar
  45. Volesky B (1990) Biosorption of heavy metals, vol M-29. CRC Press, Inc., Boca RatonGoogle Scholar
  46. Volesky B (2001) Detoxification of metal-bearing effluents: biosorption for the next century. Hydrometallurgy 59:203–216CrossRefGoogle Scholar
  47. Yan H, Yang L, Wang Q (2011) Evaluation of cadmium species lability using ion-pair reversed phase HPLC coupled on-line with inductively coupled plasma mass spectrometry. Talanta 84:287–292. doi: 10.1016/j.talanta.2011.01.019 CrossRefGoogle Scholar
  48. Zhu CJ, Lee YK (1997) Determination of biomass dry weight of marine microalgae. J Appl Phycol 9:189–194CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Enrique Torres
    • 1
    Email author
  • Roi Mera
    • 1
  • Concepción Herrero
    • 1
  • Julio Abalde
    • 1
  1. 1.Laboratorio de Microbiología, Facultad de CienciasUniversidade da CoruñaLa CoruñaSpain

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