Skip to main content
Log in

Toxic metals accumulation in Trichoderma asperellum and T. harzianum

  • Experimental Articles
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract

Heavy metal contamination represents an important environmental issue due to the toxic effects of metals on different organisms. Filamentous fungi play an important impact in the bioremediation of heavy metal-contaminated wastewater and soil. The purpose of this investigation was to observe fungal uptake behavior toward heavy metal. For this aim Trichoderma asperellum TS141 and T. harzianum TS103 at growth period were screened for their tolerance and uptake capability of cadmium (Cd), lead (Pb) and nickel (Ni) at different concentrations (0, 25, 50, 100, and 200 mg/L) in PDB media (potato dextrose broth as a complex medium). Results showed that both fungi were able to survive at the maximum concentration of 200 mg/L of the heavy metals, and remove them. T. asperellum had a better uptake capacity for Cd compared to Pb and Ni in the highest metal concentration in media. Maximum removal efficiency of Pb (68.4%) at 100 mg/L and Ni (78%) at 200 mg/L was performed by T. asperellum. For Cd, the highest removal efficiency (82.1%) was recorded by T. harzianum at 200 mg/L Cd in aqueous solution. The uptake of Cd was highly dependent on pH of solution than Pb and Ni so that the optimal pH of Cd uptake was 9 for T. asperellum and 4 for T. harzianum. Also, optimal temperature was 35°C for Cd and Pb uptake in both fungi, whereas for Ni uptake was 30 and 35°C in T. harzianum and T. asperellum, respectively. We propose that T. asperellum TS141 and T. harzianum TS103 can be used as a bioremediation agent for metal remediation from wastewater and heavy metal-contaminated soils.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Atanasova, L., Le Crom, S., Gruber, S., Coulpier, F., Seidl-Seiboth, V., Kubicek, C.P., and Druzhinina, I.S., Comparative transcriptomics reveals different strategies of Trichoderma mycoparasitism, BMC Genomics, 2013, vol. 14, p. 121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Babu, A.G., Shim, J., Bang, K.S., Shea, P.J., and Oh, B.T., Trichoderma virens PDR-28: a heavy metal-tolerant and plant growth-promoting fungus for remediation and bioenergy crop production on mine tailing soil, J. Environ. Manage., 2014, vol. 132, pp. 129–134.

    Article  CAS  PubMed  Google Scholar 

  • Baldrian, P., Interactions of heavy metals with white-rot fungi, Enzyme Microb. Technol., 2003, vol. 32, pp. 78–91.

    Article  CAS  Google Scholar 

  • Beveridge, T.G., The immobilization of soluble metals by bacterial walls, Biotechnol. Bioeng., 1986, vol. 16, pp. 127–140.

    CAS  Google Scholar 

  • Chergui, A., Simultaneous biosorption of Cu, Zn, and Cr from aqueous solution by Streptomyces rimosus biomass, Bioresour. Technol., 2007, vol. 206, pp. 179–184.

    CAS  Google Scholar 

  • Congeevaram, S., Dhanarani, S., Park, J., Dexilin, M., and Thamaraiselvi, K., Biosorption of chromium and nickel by heavy metal resistant fungal and bacterial isolates, J. Hazard. Mater., 2007, vol. 146, pp. 270–277.

    Article  CAS  PubMed  Google Scholar 

  • Das, S.K., Biosorption of cadmium, copper and chromium by Termitomyces clypeatus, Colloids Surf. B, 2007, vol. 60, pp. 46–54.

    Article  CAS  Google Scholar 

  • Dönmez, G. and Aksu, Z., Bioaccumulation of copper(II) and nickel(II) by the non-adapted and adapted growing Candida sp., Water Res., 2001, vol. 35, pp. 1425–1434.

    Article  PubMed  Google Scholar 

  • dos Santos, R.W., Schmidt, É.C., Marthiellen, R.L., Polo, L.K., Kreusch, M., Pereira, D.T., Costa, G.B., Simioni, C., Chow, F., and Ramlov, F., Bioabsorption of cadmium, copper and lead by the red macroalga Gelidium floridanum: physiological responses and ultrastructure features, Ecotoxicol. Environ. Saf., 2014, vol. 105, pp. 80–89.

    Article  PubMed  Google Scholar 

  • Edris, G., Alhamed, Y., and Alzahrani, A., Biosorption of cadmium and lead from aqueous solutions by Chlorella vulgaris biomass: equilibrium and kinetic study, Arab. J. Sci. Eng., 2013, vol. 39, pp. 87–93.

    Article  Google Scholar 

  • Errasquin, E.L. and Vazquez, C., Tolerance and uptake of heavy metals by Trichoderma atroviride isolated from sludge, Chemosphere, 2003, vol. 50, pp. 137–143.

    Article  Google Scholar 

  • Goyal, N., Jaina, S.C., and Banerjee, U.C., Comparative studies on the microbial adsorption of heavy metals, Adv. Environ. Res., 2003, vol. 7, pp. 311–319.

    Article  CAS  Google Scholar 

  • Hasan, S., Hashim, M.A., and Gupta, B.S., Adsorption of Ni (SO4) on Malaysian rubber–wood ash, Bioresour. Technol., 2000, vol. 72, pp. 153–158.

    Article  CAS  Google Scholar 

  • Hlihor, R.M., Diaconu, M., Leon, F., Curteanu, S., Tavares, T., and Gavrilescu, M., Experimental analysis and mathematical prediction of Cd(II) removal by biosorption using support vector machines and genetic algorithms, New Biotechnol., 2015, vol. 32, pp. 358–368.

    Article  CAS  Google Scholar 

  • Iram, S., Shabbir, R., Zafar, H., and Javaid, M., Biosorption and bioaccumulation of copper and lead by heavy metal-resistant fungal isolates, Arab. J. Sci. Eng., 2015, vol. 40, pp. 1867–1873.

    Article  CAS  Google Scholar 

  • Iskandar, N.L., Zainudin, N.A.I.M., and Tan, S.G., Tolerance and biosorption of copper (Cu) and lead (Pb) by filamentous fungi isolated from a freshwater ecosystem, J. Environm. Sci., 2011, vol. 23, pp. 824–830.

    Article  CAS  Google Scholar 

  • Javanbakht, V., Zilouei, H., and Karimi, K., Lead biosorption by different morphologies of fungus Mucor indicus, Int. Biodeterior. Biodegradation, 2011, vol. 65, pp. 294–300.

    Article  CAS  Google Scholar 

  • Leqba, M., Biosorption of lead, copper, cadmium, and zinc ions on loofa sponge immobilized biomass of Phanerochaete chrysosporium, Miner. Eng., 2004, vol. 17, pp. 217–223.

    Article  Google Scholar 

  • Lima Ade, F., de Moura, G.F., de Lima, M.A., de Souza, P.M., da Silva, C.A., Takaki, G.M., and do Nascimento, A.E., Role of the morphology and polyphosphate in Trichoderma harzianum related to cadmium removal, Molecules, 2011, vol. 16, pp. 2486–2500.

    Article  PubMed  Google Scholar 

  • Mc Grath, S.P., Zhao, F.J., and Lombi, E., Plant and rhizosphere processes involved in phytoremediation of metalcontaminated soils, Plant Soil, 2001, vol. 232, pp. 207–214.

    Article  CAS  Google Scholar 

  • Mogollón, L., Rodríguez, R., Larrota, W., Ramirez, N., and Torres, R., Biosorption of nickel using filamentous fungi, Appl. Biochem. Biotechnol., 1998, vol. 70, pp. 593–601.

    Article  PubMed  Google Scholar 

  • Mohsenzade, F. and Shahrokhi, F., Biological removing of cadmium from contaminated media by fungal biomass of Trichoderma species, J. Environ. Health Sci. Eng., 2014, vol. 12, p. 102.

    Article  Google Scholar 

  • Munoz, R., Alvarez, M.T., Munoz, A., Terrazas, E., Guieysse, B., and Mattisasson, B., Sequential removal of heavy metals ions and organic pollutants using an algalbacterial consortium, Chemosphere, 2006, vol. 63, pp. 903–991.

    Article  CAS  PubMed  Google Scholar 

  • Nair, A., Juwarkar, A.A., and Devotta, S., Study of speciation of metals in an industrial sludge and evaluation of metal chelators for their removal, J. Hazard. Mater., 2008, vol. 52, pp. 545–553.

    Article  Google Scholar 

  • Nongmaithem, N., Roy, A., and Bhattacharya, P.M., Screening of Trichoderma isolates for their potential of biosorption of nickel and cadmium, Braz. J. Microbiol., 2016, vol. 47, pp. 305–313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nwuche, C.O. and Ugoji, E.O., Effect of heavy metal pollution on the soil microbial activity, J. Environ. Sci., 2008, vol. 5, pp. 409–414.

    CAS  Google Scholar 

  • Ozcan, A., Ozcan, A.S., Tunali, S., Akar, T., and Kiran, I., Determination of the equilibrium, kinetic and thermodynamic parameters of adsorption of copper(II) ions onto seeds of Capsicum annuum, J. Hazard. Mater., 2005, vol. 124, pp. 200–208.

    Article  PubMed  Google Scholar 

  • Pepper, I.L., Microbial responses to environmentally toxic cadmium, Microb. Ecol., 2000, vol. 38, pp. 358–364.

    Google Scholar 

  • Sahu, A., Mandal, A., Thakur, J., Manna, M.C., and Rao, A.S., Exploring bioaccumulation efficacy of Trichoderma viride: an alternative bioremediation of cadmium and lead, Nat. Acad. Sci. Lett., 2012, vol. 35, pp. 299–302.

    Article  CAS  Google Scholar 

  • Say, R., Denizli, A., and Arica, Y.M., Biosorption of cadmium(II), lead(II), and copper(II) with the filamentous fungus Phanerochaete chrysosporium, Bioresour. Technol., 2001, vol. 76, pp. 67–70.

    Article  CAS  PubMed  Google Scholar 

  • Siddiquee, S., Aishah, S., Azad, S., Sgafawati, S., and Naher, L., Tolerance and biosorption capacity of Zn2+, Pb2+, Ni3+, and Cu2+ by filamentous fungi (Trichoderma harzianum, T. aureoviride and T. virens), Adv. Biosci. Bioeng., 2013, vol. 4, pp. 570–583.

    CAS  Google Scholar 

  • Ting, A.S.Y. and Choong, C.C., Bioaccumulation and biosorption efficacy of Trichoderma isolates SP2F1 in removing copper (Cu II) from aqueous solutions, World J. Microbiol. Biotechnol., 2009, vol. 25, pp. 1431–1437.

    Article  CAS  Google Scholar 

  • Tripathi, P., Singh, P.C., Mishra, A., Chauhan, P.S., Dwivedi, S., and Tripathi, R.D., Trichoderma: a potential bioremediator for environmental clean up, Clean Technol. Envir., 2013, vol. 15, pp. 541–550.

    Article  CAS  Google Scholar 

  • Tsezos, M. and Volesky, B., Biosorption of uranium and thorium, Biotechnol. Bioeng., 1981, vol. 23, pp. 583–604.

    Article  CAS  Google Scholar 

  • Vallee, B.L. and Ulmis, P.D., Biochemical effects of mercury, cadmium and lead, Annu. Rev. Biochem., 1972, vol. 41, pp. 91–96.

    Article  CAS  PubMed  Google Scholar 

  • Xiao, X., Luo, S., Zeng, G., Wie, W., Wan, Y., Chen, L., Guo, H., Yang, L., Chen, J., and Xi, Q., Biosorption of cadmium by endophytic fungus (EF) Microsphaeropsis sp. LSE10 isolated from cadmium hyperaccumulator Solanum nigrum L., Bioresour. Technol., 2010, vol. 101, pp. 1668–1674.

    Article  CAS  PubMed  Google Scholar 

  • Yalcin, E., Cavusoglu, K., and Kinalioglu, K., Biosorption of Cu2+ and Zn2+ by raw and autoclaved Rocella phycopsis, J. Environ. Sci., 2010, vol. 22, pp. 367–373.

    Article  CAS  Google Scholar 

  • Yeo, I.W., Roh, Y., Lee, K., et al., Arsenic reduction and precipitation by Shewanella sp.: batch and column tests, Geosci. J., 2008, vol. 12, pp. 151–157.

    Article  Google Scholar 

  • Zafar, S., Aqil, F., and Ahmad, I., Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agricultural soil, Bioresour. Technol., 2007, vol. 98, pp. 2557–2561.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Shahabivand.

Additional information

The article is published in the original.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hoseinzadeh, S., Shahabivand, S. & Aliloo, A.A. Toxic metals accumulation in Trichoderma asperellum and T. harzianum. Microbiology 86, 728–736 (2017). https://doi.org/10.1134/S0026261717060066

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261717060066

Keywords

Navigation