Skip to main content
SpringerLink
Log in

Mycoremediation: a treatment for heavy metal-polluted soil using indigenous metallotolerant fungi

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Bioleaching of heavy metals from industrial contaminated soil using metallotolerant fungi is the most efficient, cost-effective, and eco-friendly technique. In the current study, the contaminated soil samples from Hattar Industrial Estate revealed a total lead (Pb) and mercury (Hg) concentration of 170.90 mg L−1 and 26.66 mg L−1, respectively. Indigenous metallotolerant fungal strains including Aspergillus niger M1, Aspergillus fumigatus M3, Aspergillus terreus M6, and Aspergillus flavus M7 were isolated and identified by pheno- and genotyping. A. fumigatus and A. flavus of soil sample S1 showed higher efficiency for Pb removal (99.20% and 99.30%, respectively), in SDB medium. Likewise, A. niger and A. terreus of soil sample S2 showed higher efficiency for Hg removal (96% and 95.50%, respectively), in YPG medium. Furthermore, the maximum uptake efficiency for Pb removal (8.52 mg g−1) from soil sample S1 was noticed for A. fumigatus in YPG medium, while the highest uptake efficiency (4.23 mg g−1) of A. flavus M2 strain was observed with CYE medium. Similarly, the maximum uptake efficiency of 0.41 mg g−1 and 0.44 mg g−1 for Hg removal from soil sample S2 was found for A. niger and A. terreus strains, respectively, in CYE medium. Thus, in order to address the major issue of industrial waste pollution, indigenous fungal strains A. fumigatus (M1) and A. terreus (M7), isolated in this study, could be used (ex situ or in situ) to remediate soils contaminated with Pb and Hg.

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
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abd El Hameed, A. H., Eweda, W. E., Abou-Taleb, K. A. A., & Mira, H. I. (2015). Biosorption of uranium and heavy metals using some local fungi isolated from phosphatic fertilizers. Annals of Agricultural Sciences, 60(2), 345–351. https://doi.org/10.1016/j.aoas.2015.10.003.

    Article  Google Scholar 

  • Abraham, J., Dowling, K., & Florentine, S. (2018). Controlled burn and immediate mobilization of potentially toxic elements in soil, from a legacy mine site in Central Victoria, Australia. Science of The Total Environment, 616, 1022–1034.

    Article  Google Scholar 

  • Al-Samarrai, T., & Schmid, J. (2000). A simple method for extraction of fungal genomic DNA. Letters in Applied Microbiology, 30(1), 53–56.

    Article  CAS  Google Scholar 

  • Anand, P., Isar, J., Saran, S., & Saxena, R. K. (2006a). Bioaccumulation of copper by Trichoderma viride. Bioresource Technology, 97(8), 1018–1025. https://doi.org/10.1016/j.biortech.2005.04.046.

    Article  CAS  Google Scholar 

  • Anand, P., Isar, J., Saran, S., & Saxena, R. K. (2006b). Bioaccumulation of copper by Trichoderma viride. Bioresource Technology, 97(8), 1018–1025. https://doi.org/10.1016/j.biortech.2005.04.046.

    Article  CAS  Google Scholar 

  • Bahaloo-Horeh, N., Mousavi, S. M., & Baniasadi, M. (2018). Use of adapted metal tolerant Aspergillus niger to enhance bioleaching efficiency of valuable metals from spent lithium-ion mobile phone batteries. Journal of Cleaner Production., 197, 1546–1557.

    Article  CAS  Google Scholar 

  • Barrech, D., Ali, I., & Tareen, M. (2018). 1. A review on mycoremediation—the fungal bioremediation. Pure and Applied Biology (PAB), 7(1), 343–348.

    Google Scholar 

  • Brierley, C. L. (1990). Bioremediation of metal-contaminated surface and groundwaters. Geomicrobiology Journal, 8(3-4), 201–223. https://doi.org/10.1080/01490459009377894.

    Article  CAS  Google Scholar 

  • Chai, L., Yang, Z., Shi, Y., Liao, Q., Min, X., Li, Q., et al. (2018). Cr (VI)-reducing strain and its application to the microbial remediation of Cr (VI)-contaminated soils. In Twenty years of research and development on soil pollution and remediation in China (pp. 487-498). Springer.

  • Chanteperdrix, V., Bourgerette, E., Gantier, J., Herman, D., & Lauby, M. (2008) Mycological examination of a non-uniseriate Fumigati section's Aspergillus. In Annales de biologie clinique (Vol. 66, pp. 581-583, Vol. 5)

  • Chen, H., & Pan, S.-s. (2005). Bioremediation potential of spirulina: toxicity and biosorption studies of lead. Journal of Zhejiang University. Science. B, 6(3), 171.

    Article  CAS  Google Scholar 

  • Chowdhury, M. A. H., Hoque, M. M., Naher, K., Islam, M., Tamim, U., Alam, K., et al. (2017). Analysis of heavy metals and other elements in textile waste using neutron activation analysis and atomic absorption spectrophotometry. Journal of Environmental Science, Toxicology and Food Technology, 11, 14.

    Article  CAS  Google Scholar 

  • Das, A., & Osborne, J. W. (2018). Bioremediation of heavy metals. In Nanotechnology, food security and water treatment (pp. 277-311). Springer.

  • El Hameed, A. H. A., Eweda, W. E., Abou-Taleb, K. A., & Mira, H. (2015). Biosorption of uranium and heavy metals using some local fungi isolated from phosphatic fertilizers. Annals of Agricultural Sciences, 60(2), 345–351.

    Article  Google Scholar 

  • Faraji, F., Golmohammadzadeh, R., Rashchi, F., & Alimardani, N. (2018). Fungal bioleaching of WPCBs using Aspergillus niger: observation, optimization and kinetics. Journal of Environmental Management, 217, 775–787.

    Article  CAS  Google Scholar 

  • Faryal, R., Sultan, A., Tahir, F., Ahmed, S., & Hameed, A. (2007). Biosorption of lead by indigenous fungal strains. Pakistan Journal of Botany, 39(2), 615.

    Google Scholar 

  • Fernández, P. M., Viñarta, S. C., Bernal, A. R., Cruz, E. L., & Figueroa, L. I. (2018). Bioremediation strategies for chromium removal: current research, scale-up approach and future perspectives. Chemosphere., 208, 139–148.

    Article  Google Scholar 

  • Gautam, S., Bundela, P., Pandey, A., Awasthi, M., & Sarsaiya, S. (2011). Isolation, identification and cultural optimization of indigenous fungal isolates as a potential bioconversion agent of municipal solid waste. Annals of Environmental Science, 5(1), 4.

    Google Scholar 

  • Gopinath, A., Krishna, K., & Karthik, C. (2020). Adsorptive removal and recovery of heavy metal ions from aqueous solution/effluents using conventional and non-conventional materials. In Modern age waste water problems (pp. 309-328). Springer.

  • Hietala, K. A., & Roane, T. M. (2009). Microbial remediation of metals in soils. In A. Singh, R. C. Kuhad, & O. P. Ward (Eds.), Advances in applied bioremediation (pp. 201–220). Berlin, Heidelberg: Springer Berlin Heidelberg.

    Chapter  Google Scholar 

  • Hussain, Z., Chaudhry, M. R., Zuberi, F. A., Hussain, Q., & Sharif, M. (1996). Contaminants and the soil environment of Pakistan. In R. Naidu, R. S. Kookana, D. P. Oliver, S. Rogers, & M. J. McLaughlin (Eds.), Contaminants and the soil environment in the Australasia-Pacific Region: proceedings of the first Australasia-Pacific Conference on Contaminants and Soil Environment in the Australasia-Pacific Region, held in Adelaide, Australia, 18–23 February 1996 (pp. 629-646). Dordrecht: Springer Netherlands.

  • Iheanacho, H. E., Njobeh, P. B., Dutton, F. M., Steenkamp, P. A., Steenkamp, L., Mthombeni, J. Q., Daru, B. H., & Makun, A. H. (2014). Morphological and molecular identification of filamentous Aspergillus flavus and Aspergillus parasiticus isolated from compound feeds in South Africa. Food Microbiology, 44, 180–184.

    Article  CAS  Google Scholar 

  • Iskandar, N. L., Zainudin, N. A. I. M., & Tan, S. G. (2011). Tolerance and biosorption of copper (Cu) and lead (Pb) by filamentous fungi isolated from a freshwater ecosystem. Journal of Environmental Sciences, 23(5), 824–830. https://doi.org/10.1016/S1001-0742(10)60475-5.

    Article  CAS  Google Scholar 

  • Iwamoto, T., & Nasu, M. (2001). Current bioremediation practice and perspective. Journal of Bioscience and Bioengineering, 92(1), 1–8. https://doi.org/10.1016/S1389-1723(01)80190-0.

    Article  CAS  Google Scholar 

  • Javanbakht, V., Alavi, S. A., & Zilouei, H. (2014). Mechanisms of heavy metal removal using microorganisms as biosorbent. Water Science and Technology, 69(9), 1775–1787.

    Article  CAS  Google Scholar 

  • Jobby, R., Jha, P., Yadav, A. K., & Desai, N. (2018). Biosorption and biotransformation of hexavalent chromium [Cr (VI)]: a comprehensive review. Chemosphere, 207, 255–266.

    Article  CAS  Google Scholar 

  • Khan, A. G. (2001). Relationships between chromium biomagnification ratio, accumulation factor, and mycorrhizae in plants growing on tannery effluent-polluted soil. Environment International, 26(5-6), 417–423.

    Article  CAS  Google Scholar 

  • Khan, I., Nazir, K., Wang, Z.-P., Liu, G.-L., & Chi, Z.-M. (2014). Calcium malate overproduction by Penicillium viticola 152 using the medium containing corn steep liquor. Applied Microbiology and Biotechnology, 98(4), 1539–1546.

    Article  CAS  Google Scholar 

  • Khan, I., Qayyum, S., Ahmed, S., Haleem, K. S., Liu, G.-L., & Chi, Z.-M. (2017). Isolation and characterization of medicinally important marine Penicillium isolates. Pakistan Journal of Zoology, 49(2).

  • Khodja, H., Iddou, A., Aguedal, H., Aziz, A., & Shishkin, A. (2018). Bioremoval of lead (II) and cadmium (II) in single and multicomponent systems using Penicillium sp. In Key Engineering Materials (Vol. 762, pp. 93-98). Trans Tech Publ.

  • Kumar, V. (2018). Mechanism of microbial heavy metal accumulation from a polluted environment and bioremediation. In Microbial cell factories (pp. 149-174). CRC Press.

  • Lass-Florl, C. (2012). Aspergillus terreus: how inoculum size and host characteristics affect its virulence. The Journal of Infectious Diseases, 205(8), 1192–1194. https://doi.org/10.1093/infdis/jis185.

    Article  Google Scholar 

  • Muñoz, A., Ruiz, E., Abriouel, H., Gálvez, A., Ezzouhri, L., Lairini, K., et al. (2012). Heavy metal tolerance of microorganisms isolated from wastewaters: identification and evaluation of its potential for biosorption. Chemical Engineering Journal, 210, 325–332.

    Article  Google Scholar 

  • Nair, S., & Abraham, J. (2018). Hazardous waste management with special reference to biological treatment.

  • O’Sullivan, T. M. (2018). Environmental security and public health. In Introduction to homeland security (pp. 203-236). Routledge.

  • Ong, G. H., Leeraj, C., Soh, J., & Wong, L. S. (2017). Isolation and identification of fungi from polluted soil in Peninsular Malaysia for copper remediation. Pollution Research Paper, 36(1), 18–21.

    CAS  Google Scholar 

  • Pan, X., Achal, V., Zhao, C., Yang, J., & Kumari, D. (2018). Microbial remediation of heavy metals and arsenic-contaminated environments in the arid zone of northwest China. In Twenty years of research and development on soil pollution and remediation in China (pp. 477-486). Springer.

  • Pandey, A., Tripathi, P. H., Pandey, S. C., Pathak, V. M., & Nailwal, T. K. (2018). Removal of toxic pollutants from soil using microbial biotechnology. In Microbial biotechnology in environmental monitoring and cleanup (pp. 86-105). IGI Global.

  • Park, S.-W., Lee, J.-Y., Yang, J.-S., Kim, K.-J., & Baek, K. (2009). Electrokinetic remediation of contaminated soil with waste-lubricant oils and zinc. Journal of Hazardous Materials, 169(1), 1168–1172. https://doi.org/10.1016/j.jhazmat.2009.04.039.

    Article  CAS  Google Scholar 

  • Pedersen, L. H., Skouboe, P., Boysen, M., Soule, J., & Rossen, L. (1997). Detection of Penicillium species in complex food samples using the polymerase chain reaction. International Journal of Food Microbiology, 35(2), 169–177.

    Article  CAS  Google Scholar 

  • Penny, C., Vuilleumier, S., & Bringel, F. (2010). Microbial degradation of tetrachloromethane: mechanisms and perspectives for bioremediation. FEMS Microbiology Ecology, 74(2), 257–275. https://doi.org/10.1111/j.1574-6941.2010.00935.x.

    Article  CAS  Google Scholar 

  • Pitt, J. I., & Samson, R. A. (2014). Integration of modern taxonomic methods for Penicillium and Aspergillus classification. CRC Press.

  • Qayyum, S., Khan, I., Bhatti, Z. A., Tang, F., & Peng, C. (2016a). Fungal strain Aspergillus flavus F3 as a potential candidate for the removal of lead (II) and chromium (VI) from contaminated soil. Main Group Metal Chemistry, 39(3-4), 93–104.

    Article  CAS  Google Scholar 

  • Qayyum, S., Khan, I., Maqboo, F., Zhao, Y., Gu, Q., & Peng, C. (2016b). Isolation and characterization of heavy metal resistant fungal isolates from industrial soil in China. Pakistan Journal of Zoology, 48(5).

  • Qayyum, S., Khan, I., Meng, K., Zang, X., Zhao, Y., Gu, Q., et al. (2016c). Bioaccumulation of heavy metals from aqueous solution using indigenous fungal isolates. Indian Journal of Geo-Marine Sciences, 45(4), 499–507.

    Google Scholar 

  • Rehman, A., Jingdong, L., Shahzad, B., Chandio, A. A., Hussain, I., Nabi, G., & Iqbal, M. S. (2015). Economic perspectives of major field crops of Pakistan: an empirical study. Pacific Science Review B: Humanities and Social Sciences, 1(3), 145–158. https://doi.org/10.1016/j.psrb.2016.09.002.

    Article  Google Scholar 

  • Samson, R. A., & Pitt, J. I. (2000). Integration of modern taxonomic methods for Penicillium and Aspergillus classification. Taylor & Francis.

  • Sanyal, A., Rautaray, D., Bansal, V., Ahmad, A., & Sastry, M. (2005). Heavy-metal remediation by a fungus as a means of production of lead and cadmium carbonate crystals. Langmuir, 21(16), 7220–7224. https://doi.org/10.1021/la047132g.

    Article  CAS  Google Scholar 

  • Sanyaolu, A. A. A. (2018). Verification of Aspergillus niger as a myco-remediation agent of lambda-cyhalothrin and associated heavy metals in Lactuca sativa (L.) leaf. Journal of Applied Sciences and Environmental Management, 22(5), 621–624.

    Article  Google Scholar 

  • Schultze-Lam, S., Urrutia-Mera, M., & Beveridge, T. J. (2018). Metal and silicate sorption and subsequent mineral formation on bacterial surfaces: subsurface implications. In Metal contaminated aquatic sediments (pp. 111-147). Routledge.

  • Sen, M. (2018). Enhanced biological removal of Cr (VI) in continuous stirred tank reactor (CSTR) using Aspergillus sp. Brazilian Journal of Biological Sciences, 5(9), 33–45.

    Article  Google Scholar 

  • Singh, P. C., Srivastava, S., Shukla, D., Bist, V., Tripathi, P., Anand, V., et al. (2018). Mycoremediation mechanisms for heavy metal resistance/tolerance in plants. In Mycoremediation and environmental sustainability (pp. 351-381). Springer.

  • Smith, J., & Doran, J. (1996). Measurement and use of pH and electrical conductivity for soil quality analysis. Methods for assessing soil quality, 49.

  • Su, S. L., Singh, D., & Baghini, M. S. (2014). A critical review of soil moisture measurement. Measurement, 54, 92–105.

    Article  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30(12), 2725–2729.

    Article  CAS  Google Scholar 

  • Tchounwou, P. B., Yedjou, C. G., Patlolla, A. K., & Sutton, D. J. (2012). Heavy metal toxicity and the environment. In Molecular, clinical and environmental toxicology (pp. 133-164). Springer.

  • Upadhyay, A. K., Singh, R., & Singh, D. (2019). Phycotechnological approaches toward wastewater management. In Emerging and eco-friendly approaches for waste management (pp. 423-435). Springer.

  • Zafar, S., Aqil, F., & Ahmad, I. (2007). Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agricultural soil. Bioresource Technology, 98(13), 2557–2561.

    Article  CAS  Google Scholar 

  • Zhang, X.-h., Wang, H., & Luo, Q.-s. (2001). Electrokinetics in remediation of contaminated groundwater and soils. Advances In Water Science, 12(2), 249–255.

    CAS  Google Scholar 

  • Zhang, W., Jiang, F., & Ou, J. (2011). Global pesticide consumption and pollution: with China as a focus. Proceedings of the International Academy of Ecology and Environmental Sciences, 1(2), 125.

    CAS  Google Scholar 

  • Zolfaghari, G. (2018). Risk assessment of mercury and lead in fish species from Iranian international wetlands. MethodsX, 5, 438–447.

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the Higher Education Commission, Government of Pakistan, under SRGP Program (No: 21-1259/SRGP/R&D/HEC/2017).

Author information

Authors and Affiliations

  1. Department of Microbiology, Abbottabad University of Science & Technology, Havelian, 22010, Pakistan

    Ibrar Khan

  2. Department of Microbiology, Hazara University, Mansehra, 21300, Pakistan

    Madiha Ali, Maryam Aftab, SajidUllah Shakir, Sadia Qayyum, Kashif Syed Haleem & Isfahan Tauseef

Authors
  1. Ibrar Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Madiha Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maryam Aftab
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. SajidUllah Shakir
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sadia Qayyum
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kashif Syed Haleem
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Isfahan Tauseef
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Ibrar Khan or Isfahan Tauseef.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, I., Ali, M., Aftab, M. et al. Mycoremediation: a treatment for heavy metal-polluted soil using indigenous metallotolerant fungi. Environ Monit Assess 191, 622 (2019). https://doi.org/10.1007/s10661-019-7781-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10661-019-7781-9

Keywords

Search

Navigation