Annals of Microbiology

, Volume 63, Issue 2, pp 503–511 | Cite as

Sorption of lead and copper from an aqueous phase system by marine-derived Aspergillus species

  • Mufeda A. H. Gazem
  • Sarita Nazareth
Original Article


A total of 47 cultures of Aspergillus representing 13 species were screened for their ability to tolerate 7.5 mM Pb2+ and 2 mM Cu2+, all of which were positive, with growth of 31 of the cultures being enhanced by low concentrations of lead. The isolates of Aspergillus versicolor, A. niger and A. flavus were tolerant to concentrations as high as 10 - 12.5 mM Pb2+ and 3 – 4 mM Cu2+. Selected cultures displayed a good sorption capacity of 32 - 41 mg Pb2+ and 3.5 - 6.5 mg Cu2+ g-1 dry weight of mycelia, which was improved by alkali pretreatment of the biomass and negatively affected by mild dry heat treatment. The sequestration of the metal occurred mainly by sorption to the cell-surface with very little intracellular uptake. FTIR analysis indicated the involvement of hydroxyl, amino, and carbonyl groups in Pb2+ and Cu2+ biosorption by fungal biomass of the different species of Aspergillus.


Aspergillus Heavy metals Biosorption Cell wall Functional groups 



The authors are grateful to S. Tilve and P. Torney, Department of Chemistry, Goa University for the FTIR analysis. The scholarship to M. Gazem from the University of Taiz is gratefully acknowledged.


  1. Acemioğlu B, Kertmen M, Diğrak M, Alma HM (2010) Use of Aspergillus wentii for biosorption of methylene blue from aqueous solution. Afr J Biotechnol 9(6):874–881Google Scholar
  2. Ahuja P, Mohapatra H, Saxena RK, Gupta R (2001) Reduced uptake as a mechanism of zinc tolerance in Oscillatoria anguistissima. Curr Microbiol 43:305–10PubMedCrossRefGoogle Scholar
  3. Akar T, Tunali S (2006) Biosorption characteristics of Aspergillus flavus biomass for removal of Pb(II) and Cu(II) ions from an aqueous solution. Bioresour Technol 197:1780–1787CrossRefGoogle Scholar
  4. Akar T, Tunali S, Cabuk A (2007) Study on the characterization of lead (II) biosorption by fungus Aspergillus parasiticus. Appl Biochem Biotechnol 136:389–405PubMedCrossRefGoogle Scholar
  5. Akhtar MN, Sastry KS, Mohan PM (1996) Mechanism of metal ion biosorption by fungal biomass. Biometals 9:21–28Google Scholar
  6. Al-Garni S, Ghanem KM, Bahobail AS (2009) Biosorption characteristics of Aspergillus fumigatus in removal of cadmium from an aqueous solution. Afr J Biotechnol 8:4163–4172Google Scholar
  7. Al-Kadeeb AS (2007) Effect of lead and copper on the growth of heavy metal resistance fungi isolated from second industrial city in Riyadh, Saudi Arabia. J App Sci 7:1019–1024CrossRefGoogle Scholar
  8. Anand P, Isar J, Saran S, Saxena RK (2006) Bioaccumulation of copper by Trichoderma viride. Bioresour Technol 97:1018–1025PubMedCrossRefGoogle Scholar
  9. Ashkenazy R, Gottlieb L, Yannai S (1997) Characterization of acetone-washed yeast biomass functional groups involved in lead biosorption. Biotechnol Bioeng 55:1–10PubMedCrossRefGoogle Scholar
  10. Aung KM, Ting YP (2005) Bioleaching of spent fluid catalytic cracking catalyst using Aspergillus niger. J Biotechnol 116:159–170PubMedCrossRefGoogle Scholar
  11. Baik WY, Bae JH, Cho KM, Hartmeier W (2002) Biosorption of heavy metals using whole mold mycelia and parts thereof. Bioresour Technol 81:167–170PubMedCrossRefGoogle Scholar
  12. Bairagia H, Khan MMR, Raya L, Guhab AK (2011) Adsorption profile of lead on Aspergillus versicolor: a mechanistic probing. J Hazard Mater 186:756–764CrossRefGoogle Scholar
  13. Cabuk A, Ülhan S, Fuluk C, Alipkan F (2005) Pb2+ Biosorption by pretreated fungal biomass. Turk J Biol 29:23–28Google Scholar
  14. Company R, Serafim A, Bebianno MJ, Cosson R, Shillito B, Fiala-Medioni A (2004) Effect of cadmium, copper and mercury on antioxidant enzyme activities and lipid peroxidation in the gills of the hydrothermal vent mussel Bathymodiolus azoricus. Mar Environ Res 58:377–381PubMedCrossRefGoogle Scholar
  15. Dacera D, Babel S (2008) Removal of heavy metals from contaminated sewage sludge using Aspergillus niger fermented raw liquid from pine apple wastes. Bioresour Technol 99(6):1682–1689CrossRefGoogle Scholar
  16. Das N, Charumathi D, Vimala R (2007) Effect of pretreatment on Cd2+ biosorption by mycelial biomass of Pleurotus florida. Afr J Biotechnol 6:2555–2558Google Scholar
  17. Dias MA, Lacerda ICA, Pimentel PF, de Castro HF, Rosa CA (2002) Removal of heavy metal by an Aspergillus terreus strain immobilized in polyurethane matrix. Lett Appl Microbiol 34:46–50PubMedCrossRefGoogle Scholar
  18. Dursun AY, Uslu G, Cuci Y, Aksu Z (2003) Bioaccumulation of copper(II), lead(II) and chromium(VI) by growing Aspergillus niger. Process Biochem 38:1647–1651CrossRefGoogle Scholar
  19. Ezzouhri L, Castro E, Moya M, Espinola F, Lairini K (2009) Heavy metal tolerance of filamentous fungi isolated from polluted sites in Tangier, Morocco. Afr J Microbiol Res 32:35–48Google Scholar
  20. Feng D, Aldrich C (2004) Adsorption of heavy metals by biomaterials derived from the marine alga Ecklonia maxima Hydrometallurgy 73(1–2):1–10Google Scholar
  21. Gadd GM (1993) Interactions of fungi with toxic metals. New Phytol 124:25–60CrossRefGoogle Scholar
  22. Gadd GM (2009) Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment. J Chem Technol Biotechnol 84:13–28CrossRefGoogle Scholar
  23. Gazem MAH, Nazareth S (2012) Isotherm and kinetic models and cell surface analysis for determination of the mechanism of metal sorption by Aspergillus versicolor. World J Microbiol Biotechnol. doi: 10.1007/s11274-012-1060-z
  24. Guibal E, Roulph C, Le Cloirec P (1995) Infrared spectroscopic study of uranyl biosorption by fungal biomass and materials of biological origin. Environ Sci Technol 29:2496–2503PubMedCrossRefGoogle Scholar
  25. Huang C, Huang CP (1996) Application of Aspergillus oryzae and Rhizopus oryzae for Cu(II) removal. Water Res 30:1985–1990CrossRefGoogle Scholar
  26. Iskandar NL, Zainudin NA, Tan SG (2011) Tolerance and biosorption of copper (Cu) and lead (Pb) by filamentous fungi isolated from a freshwater ecosystem. J Environ Sci 23(5):824–830CrossRefGoogle Scholar
  27. Kapoor A, Viraraghavan T (1995) Fungal biosorption- an alternative treatment option for heavy metal bearing waste water: a review. Bioresourse Technol 53:195–206Google Scholar
  28. Kapoor A, Viraraghavan T, Cullimore DR (1999) Removal of heavy metals using the fungus Aspergillus niger. Bioresour Technol 70:95–104CrossRefGoogle Scholar
  29. Kowshik M, Nazareth S (1999) Biosorption of metals by Fusarium solani. Asian J Microbiol Biotechnol Environ Sc 1:57–61Google Scholar
  30. Kowshik M, Nazareth S (2000) Metal tolerance of Fusarium solani. Ecol Environ Conserv 6:391–395Google Scholar
  31. Leitão AL (2009) potential of Penicillium species in the bioremediation filed. Int J Environ Res Public Health 6:1393–1417PubMedCrossRefGoogle Scholar
  32. Macek T, Mackova M (2011) Potential of biosorption technology. In: Kotrba P, Mackova M, Macek T (eds) Microbial biosorption of metals. Springer, Czech Republic, pp 7–17CrossRefGoogle Scholar
  33. Marbaniang T, Nazareth S (2007) Isolation of halotolerant Penicillium species from mangroves and salterns and their resistance to heavy metals. Curr Sci 92:895–897Google Scholar
  34. Nazareth S, Marbaniang T (2008) Effect of heavy metals on cultural and morphological growth characteristics of halotololerant penicillium morphotypes. J Basic Microbiol 48:363–369PubMedCrossRefGoogle Scholar
  35. Prasenjit B, Sumathi S (2005) Uptake of chromium by Aspergillus foetidus. J Mater Cycles Waste Manag 7:88–92CrossRefGoogle Scholar
  36. Price MS, Classen JJ, Payne GA (2001) Aspergillus niger absorbs copper and zinc from swine waste water. Bioresour Technol 77:41–49PubMedCrossRefGoogle Scholar
  37. Rao KR, Rashmi K, Latha J, Mohan PM (2005) Bioremediation of toxic metal ions using biomass of Aspergillus fumigatus from fermentative waste. Indian Journal of Biotechnology 4:139–143Google Scholar
  38. Raper KB, Fennell DI (1965) The Genus Aspergillus. Williams & Wilkins, BaltimoreGoogle Scholar
  39. Rehman A, Shakoori RF, Shakoori AR (2008) Uptake of heavy metals by Stylonychia mytilus and its possible use in decontamination of industrial wastewater. World J Microbiol Biotechnol 24:47–53CrossRefGoogle Scholar
  40. Santhiya D, Ting YP (2006) Use of adapted Aspergillus niger in the bioleaching of spent refinery processing catalyst. J Biotechnol 121:62–74PubMedCrossRefGoogle Scholar
  41. Sen M, Dastidar MG, Roychoudhury PK (2005) Biosorption of Chromium (VI) by nonliving Fusarium sp. isolated from soil. J Hazard Toxic Radioac Waste 9(3):143–147Google Scholar
  42. Sun F, Shao Z (2007) Biosorption and bioaccumulation of lead by Penicillium sp. Psf-2 isolated from the deep sea sediment of the Pacific Ocean. Extremophiles 11:853–858PubMedCrossRefGoogle Scholar
  43. Sun Y, Horng C, Chang F, Chang L, Tain W (2010) Biosorption of lead, mercury and cadmium ions by Aspergillus terreus immobilized in anatural matrix. Polish J Microbiol 59(1):37–44Google Scholar
  44. Taboski MAS, Rand TG, Piórko A (2005) Lead and cadmium uptake in the marine fungi Corollospora lacera and Monodictys pelagica. FEMS Microbiol Ecol 53:445–453PubMedCrossRefGoogle Scholar
  45. Tsekova K, Todorova D, Ganeva S (2010) Removal of heavy metals from industrial wastewater by free and immobilized cells of Aspergillus niger. Int Biodeterior Biodegr 64:447–451CrossRefGoogle Scholar
  46. Vinopal S, Ruml T, Kotrba P (2007) Biosorption of Cd2+ and Zn2+ by cell surface engineered Saccharomyces cerevisiae. Int Biodeterior Biodegr 60:96–102CrossRefGoogle Scholar
  47. Volesky B, Holan ZR (1995) Biosorption of heavy metals. Biotechnol Prog 11:235–250PubMedCrossRefGoogle Scholar
  48. Waihung LO, Hong C, Kim-Hung L, Shu-Ping B (1999) A comparative investigation on the biosorption of lead by filamentous fungal biomass. Chemosphere 39(15):2723–2736CrossRefGoogle Scholar
  49. Wang Jing-S Hu, Xin-J Liu Yun-G, Shui-B X, Zheng-L B (2010) Biosorption of uranium (VI) by immobilized Aspergillus fumigatus beads. J Environ Radio 101:504–508CrossRefGoogle Scholar
  50. Wang JL, Chen C (2006) Biosorption of heavy metals by Saccharomyces cerevisiae: a review. Biotechnol Adv 24:427–451PubMedCrossRefGoogle Scholar
  51. Whistler R, Daniel TR (1985) Carbohydrates. In: Fennema Owen R (ed) Food chemistry, vol 96., p 105Google Scholar
  52. Wood JM, Wang HK (1983) Microbial resistance to heavy metals. Environ Sci Technolo 17:582–585CrossRefGoogle Scholar
  53. Xinjio D (2006) Biosorption of Cu2+ from aqueous solutions by pretreated Cladosporium sp. J Environ Biol 27(4):639–643Google Scholar
  54. Yakubu NA, Dudeney AWL (1986) In: Eccles A, Hunt S (eds) Biosorption of uranium with Aspergillus niger, in immobilization of ions by biosorption. Ellis Horwood Chichester, Uk, pp 138–200Google Scholar
  55. Yan G, Viraraghavan T (2000) Effect of pretreatment on the bioadsorption of heavy metals on Mucor rouxii. Water SA 26:119–123Google Scholar
  56. Yan G, Viraraghavan T (2003) Heavy metal removal from aquase solution by fungus Moucr rouxii. Water Res 37:4486PubMedCrossRefGoogle Scholar
  57. Yazdani M, Yap CK, Abdullah F, Tan SG (2010) An in vitro study on the adsorption, absorption and uptake capacity of Zn by the Bioremediator Trichoderma atroviride. Environment Asia 3(1):53–59Google Scholar
  58. Zafar S, Aqil F, Ahmad I (2007) Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agricultural soil. Bioresour Technol 98:2257–2261CrossRefGoogle Scholar

Copyright information

© Springer-Verlag and the University of Milan 2012

Authors and Affiliations

  1. 1.Department of Microbiology, Taleigao PlateauGoa UniversityGoaIndia

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