Skip to main content
SpringerLink
Log in

Evaluation of copper-tolerant fungi isolated from Sarcheshmeh copper mine of Iran

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Mycoremediation, a subset of bioremediation, is considered an advanced method to eliminate environmental contaminations. To identify tolerant fungi to copper contamination and study the related gene expression, sampling was carried out from the soil of “Sarcheshmeh Copper Mine,” which is one of the biggest open-cast copper mines in the world. A total of 71 fungal isolates were obtained and purified. Afterward, the inhibitory effect of different concentrations (1000, 1500, 3500, 4000, and 5500 ppm) of copper sulfate on mycelial growth was evaluated. Results indicated that only 5500 ppm of copper sulfate inhibited fungal growth compared to the control. Based on the bioassay experiments, three isolates including S3-1, S3-21, and S1-7, which were able to grow on solid and broth medium containing 5500 ppm of copper sulfate at different pH conditions, were selected and identified using molecular approaches. Also, laccase and metallothionein gene expression has been assessed in these isolates. According to the molecular identification using ITS1-5.8S- ITS2 region, isolates S3-1 and S1-7 were identified as Pleurotus eryngii, and isolate S3-21 belonged to the genus Sarocladium. In addition, P. eryngii showed laccase gene expression reduction after 8 days of exposure to copper sulfate. While in the genus Sarocladium, it increased (almost 2 times) from 6 to 8 days. Besides, metallothionein gene expression has increased from 6 to 8 days of copper sulfate treatment compared to the control which reveals its role in copper tolerance of all studied isolates. In this study, Pleurotus eryngii and Sarocladium sp. are introduced as heavy metal tolerant fungi and the related gene expression to copper tolerance was studied for the first time in Iran.

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

Data availability

Not applicable.

References

  • Avery SV (2001) Metal toxicity in yeasts and the role of oxidative stress. Adv Appl Microbiol 49:111–142

    CAS  Google Scholar 

  • Bai RS, Abraham TE (2003) Studies on chromium (VI) adsorption–desorption using immobilized fungal biomass. Bioresour Technol 87:17–26

    Google Scholar 

  • Baldrian P, Gabriel J (2002) Variability of laccase activity in the white-rot Basidiomycete Pleurotus ostreatus. Folia Microbiol (Praha) 47:385–390

    CAS  Google Scholar 

  • Bayramoğlu G, Bektaş S, Arıca MY (2003) Biosorption of heavy metal ions on immobilized white-rot fungus Trametes versicolor. J Hazard Mater 101:285–300

    Google Scholar 

  • Blaudez D, Jacob C, Turnau K et al (2000) Differential responses of ectomycorrhizal fungi to heavy metals in vitro. Mycol Res 104:1366–1371

    CAS  Google Scholar 

  • Bonilla JO, Callegari EA, Paez MD et al (2021) Characterization of copper stress response in Fusarium tricinctum M6: a metal-resistant microorganism isolated from an acid mine drainage-affected environment. J Hazard Mater 412:125216

    CAS  Google Scholar 

  • Castanera R, Pérez G, Omarini A et al (2012) Transcriptional and enzymatic profiling of Pleurotus ostreatus laccase genes in submerged and solid-state fermentation cultures. Appl Environ Microbiol 78:4037–4045

    CAS  Google Scholar 

  • Cervantes C, Gutierrez-Corona F (1994) Copper resistance mechanisms in bacteria and fungi. FEMS Microbiol Rev 14:121–137

    CAS  Google Scholar 

  • Chatterjee S, Kumari S, Rath S et al (2020) Diversity, structure and regulation of microbial metallothionein: metal resistance and possible applications in sequestration of toxic metals. Metallomics 12:1637–1655

    CAS  Google Scholar 

  • Chen M, Arato M, Borghi L et al (2018) Beneficial services of arbuscular mycorrhizal fungi–from ecology to application. Front Plant Sci 9:1270

    Google Scholar 

  • Congeevaram S, Dhanarani S, Park J et al (2007) Biosorption of chromium and nickel by heavy metal resistant fungal and bacterial isolates. J Hazard Mater 146:270–277

    CAS  Google Scholar 

  • Cornelissen S (2004) The impact of copper on filamentous fungi and yeasts present in soil. Master of Science Thesis, University of Stellenbosch, pp 98

  • Echlin P (2011) Handbook of sample preparation for scanning electron microscopy and X-ray microanalysis. Springer Sci Bus Media

  • Eyankware MO, Obasi PN (2021) A holistic review of heavy metals in water and soil in Ebonyi SE, Nigeria; with emphasis on its effects on human, plants and aquatic organisms. World News Nat Sci 38:1–19

    CAS  Google Scholar 

  • Fernández-Fueyo E, Castanera R, Ruiz-Dueñas FJ et al (2014) Ligninolytic peroxidase gene expression by Pleurotus ostreatus: differential regulation in lignocellulose medium and effect of temperature and pH. Fungal Genet Biol 72:150–161

    Google Scholar 

  • Gadd GM, Chudek JA, Foster R, Reed RH (1984) The osmotic responses of Penicillium ochro-chloron: changes in internal solute levels in response to copper and salt stress. Microbiology 130:1969–1975

    CAS  Google Scholar 

  • Galhaup C, Haltrich D (2001) Enhanced formation of laccase activity by the white-rot fungus Trametes pubescens in the presence of copper. Appl Microbiol Biotechnol 56:225–232

    CAS  Google Scholar 

  • Gönen F, Aksu Z (2009) Single and binary dye and heavy metal bioaccumulation properties of Candida tropicalis: use of response surface methodology (RSM) for the estimation of removal yields. J Hazard Mater 172:1512–1519

    Google Scholar 

  • González MA, Pavlovic I, Rojas-Delgado R, Barriga C (2014) Removal of Cu2+, Pb2+ and Cd2+ by layered double hydroxide–humate hybrid. Sorbate and sorbent comparative studies. Chem Eng J 254:605–611

    Google Scholar 

  • Hirakawa MP, Rodriguez A, Tran-Gyamfi MB et al (2023) Phenothiazines rapidly induce laccase expression and lignin-degrading properties in the white-rot fungus Phlebia radiata. J Fungi 9:371

    CAS  Google Scholar 

  • Iram S, Arooj A, Parveen K (2012) Tolerance potential of fungi isolated from polluted soil of Multan, Pakistan. Int J Biosci 2:27–34

    Google Scholar 

  • Iskandar NL, Zainudin NAIM, Tan SG (2011) Tolerance and biosorption of copper (Cu) and lead (Pb) by filamentous fungi isolated from a freshwater ecosystem. J Environ Sci 23:824–830

    CAS  Google Scholar 

  • Jacob JM, Karthik C, Saratale RG et al (2018) Biological approaches to tackle heavy metal pollution: a survey of literature. J Environ Manage 217:56–70

    CAS  Google Scholar 

  • Kägi JHR, Kojima Y (1987) Chemistry and biochemistry of metallothionein. In: Metallothionein II. Springer, pp 25–61

  • Kapahi M, Sachdeva S (2019) Bioremediation options for heavy metal pollution. J Heal Pollut 9:191203

    Google Scholar 

  • Khan A, Rashid A, Younas R, Chong R (2016) A chemical reduction approach to the synthesis of copper nanoparticles. Int Nano Lett 6:21–26

    CAS  Google Scholar 

  • Khan I, Saeed K, Khan I (2019) Nanoparticles: properties, applications and toxicities. Arab J Chem 12:908–931

    CAS  Google Scholar 

  • Kumar KS, Dayananda S, Subramanyam C (2005) Copper alone, but not oxidative stress, induces copper–metallothionein gene in Neurospora crassa. FEMS Microbiol Lett 242:45–50

    CAS  Google Scholar 

  • Lerch K (1980) Copper metallothionein, a copper-binding protein from Neurospora crassa. Nature 284:368–370

    CAS  Google Scholar 

  • Levinskaite L (2001) Effect of heavy metals on the individual development of two fungi from the genus Penicillium. Biologija 1:25–30

    Google Scholar 

  • Liaquat F, Munis MFH, Haroon U et al (2020) Evaluation of metal tolerance of fungal strains isolated from contaminated mining soil of Nanjing. China Biology (basel) 9:469

    CAS  Google Scholar 

  • Liaquat F, Haroon U, Munis MFH et al (2021) Efficient recovery of metal tolerant fungi from the soil of industrial area and determination of their biosorption capacity. Environ Technol Innov 21:101237

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    CAS  Google Scholar 

  • Lodeiro P, Barriada JL, Herrero R, De Vicente MES (2006) The marine macroalga Cystoseira baccata as biosorbent for cadmium(II) and lead(II) removal: kinetic and equilibrium studies. Environ Pollut 142:264–273

    CAS  Google Scholar 

  • Lotlikar N, Damare S, Meena RM, Jayachandran S (2020) Variable protein expression in marine-derived filamentous fungus Penicillium chrysogenum in response to varying copper concentrations and salinity. Metallomics 12:1083–1093

    CAS  Google Scholar 

  • Mate D, García-Burgos C, García-Ruiz E et al (2010) Laboratory evolution of high-redox potential laccases. Chem Biol 17:1030–1041

    CAS  Google Scholar 

  • Medfu Tarekegn M, Zewdu Salilih F, Ishetu AI (2020) Microbes used as a tool for bioremediation of heavy metal from the environment. Cogent Food Agric 6:1783174

    Google Scholar 

  • Mishra A, Malik A (2012) Simultaneous bioaccumulation of multiple metals from electroplating effluent using Aspergillus lentulus. Water Res 46:4991–4998

    CAS  Google Scholar 

  • Mohammadian E, Ahari AB, Arzanlou M et al (2017) Tolerance to heavy metals in filamentous fungi isolated from contaminated mining soils in the Zanjan Province. Iran Chemosphere 185:290–296

    CAS  Google Scholar 

  • Montllor-Albalate C, Colin AE, Chandrasekharan B et al (2019) Extra-mitochondrial Cu/Zn superoxide dismutase (Sod1) is dispensable for protection against oxidative stress but mediates peroxide signaling in Saccharomyces cerevisiae. Redox Biol 21:101064

    CAS  Google Scholar 

  • Mtibaà R, Ezzanad A, Aranda E et al (2020) Biodegradation and toxicity reduction of nonylphenol, 4-tert-octylphenol and 2,4-dichlorophenol by the ascomycetous fungus Thielavia sp HJ22: identification of fungal metabolites and proposal of a putative pathway. Sci Total Environ 708:135129

    Google Scholar 

  • Nanda M, Sharma D, Kumar A (2011) Removal of heavy metals from industrial effluent using bacteria. Int J Environ Sci 2:765–780

    Google Scholar 

  • Neifar M, Maktouf S, Ghorbel RE et al (2015) Extremophiles as source of novel bioactive compounds with industrial potential. Biotechnol Bioact Compd sources Appl Wiley, Hoboken 245–268

  • Palanivel TM, Pracejus B, Novo LAB (2023) Bioremediation of copper using indigenous fungi Aspergillus species isolated from an abandoned copper mine soil. Chemosphere 314:137688

    CAS  Google Scholar 

  • Palmieri G, Giardina P, Bianco C et al (2000) Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Appl Environ Microbiol 66:920–924

    CAS  Google Scholar 

  • Peerzada S, Viswanath H, Bhat K (2020) In-vitro studies on effect of fungicides against mycelial growth and sporangial germination of Phytophthora infestans (Mont) de Bary) causing late blight of potato. Int J Chem Stud 8:2069–2075

    CAS  Google Scholar 

  • Pezzella C, Autore F, Giardina P et al (2009) The Pleurotus ostreatus laccase multi-gene family: isolation and heterologous expression of new family members. Curr Genet 55:45–57

    CAS  Google Scholar 

  • Priya AK, Gnanasekaran L, Dutta K et al (2022) Biosorption of heavy metals by microorganisms: evaluation of different underlying mechanisms. Chemosphere 307:135957

    CAS  Google Scholar 

  • Priyadarshini E, Priyadarshini SS, Cousins BG, Pradhan N (2021) Metal-fungus interaction: review on cellular processes underlying heavy metal detoxification and synthesis of metal nanoparticles. Chemosphere 274:129976

    CAS  Google Scholar 

  • Razzak SA, Faruque MO, Alsheikh Z et al (2022) A comprehensive review on conventional and biological-driven heavy metals removal from industrial wastewater. Environ Adv 7:100168

    CAS  Google Scholar 

  • Saeed MU, Hussain N, Sumrin A et al (2022) Microbial bioremediation strategies with wastewater treatment potentialities – a review. Sci Total Environ 818:151754

    CAS  Google Scholar 

  • Safaei N, Alizadeh AA, Saeidi A et al (2005) Molecular characterization and genetic diversity among iranian populations of Fusarium graminearum, the causal agent of wheat headblight. Iran J Plant Pathol 1:171–189

    Google Scholar 

  • Sharma P, Pandey AK, Udayan A, Kumar S (2021) Role of microbial community and metal-binding proteins in phytoremediation of heavy metals from industrial wastewater. Bioresour Technol 326:124750

    CAS  Google Scholar 

  • Shutova VV, Revin VV, Myakushina YA (2008) The effect of copper ions on the production of laccase by the fungus Lentinus (Panus) tigrinus. Appl Biochem Microbiol 44:619–623

    CAS  Google Scholar 

  • Sjaarda CP, Abubaker KS, Castle AJ (2015) Induction of lcc2 expression and activity by Agaricus bisporus provides defence against Trichoderma aggressivum toxic extracts. Microb Biotechnol 8:918–929

    CAS  Google Scholar 

  • Song J, Shen Q, Wang L et al (2018) Effects of Cd, Cu, Zn and their combined action on microbial biomass and bacterial community structure. Environ Pollut 243:510–518

    CAS  Google Scholar 

  • Tang J, Zhang J, Ren L et al (2019) Diagnosis of soil contamination using microbiological indices: a review on heavy metal pollution. J Environ Manage 242:121–130

    CAS  Google Scholar 

  • Tripathi AK, Kohli S (2013) Anti-diabetic activity and phytochemical screening of crude extracts of PuerariaTuberosa DC. (FABACEAE) grown in India on STZ-induced diabetic rats. Asian J Med Pharm Res 3:66–73

    Google Scholar 

  • Tufail MA, Iltaf J, Zaheer T et al (2022) Recent advances in bioremediation of heavy metals and persistent organic pollutants: a review. Sci Total Environ 850:157961

  • Viraraghavan T, Srinivasan A (2011) Fungal biosorption and biosorbents. In: Microbial biosorption of metals. Springer, pp 143–158

  • Vrsanska M, Voberkova S, Langer V et al (2016) Induction of laccase, lignin peroxidase and manganese peroxidase activities in white-rot fungi using copper complexes. Molecules 21:1553

  • Wang X, Pecoraro L (2021) Analysis of soil fungal and bacterial communities in Tianchi Volcano crater, northeast China. Life 11:280

    Google Scholar 

  • Welch JW, Fogel S, Cathala G, Karin M (1983) Industrial yeasts display tandem gene iteration at the CUP1 region. Mol Cell Biol 3:1353–1361

    CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protoc a Guid to Methods Appl 18:315–322

    Google Scholar 

  • Yadav S, Mishra A (2022) Fungal biosorption of the heavy metals chromium(VI) and nickel from industrial effluent-contaminated soil. J Appl Nat Sci 14:233–239

    CAS  Google Scholar 

  • Yaghoubian Y, Siadat SA, Telavat MRM et al (2019) Bio-removal of cadmium from aqueous solutions by filamentous fungi: Trichoderma spp. and Piriformospora indica. Environ Sci Pollut Res 26:7863–7872

    CAS  Google Scholar 

  • Yin Y, Wang X, Hu Y et al (2023) Soil bacterial community structure in the habitats with different levels of heavy metal pollution at an abandoned polymetallic mine. J Hazard Mater 442:130063

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Zhao J, Csetenyi L, Gadd GM (2020) Biocorrosion of copper metal by Aspergillus niger. Int Biodeterior Biodegradation 154:105081

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biotechnology, Faculty of Agriculture, Shahrood University of Technology, Shahrood, Iran

    Ferdos Ganji

  2. Department of Horticulture and Plant Protection, Faculty of Agriculture, Shahrood University of Technology, Shahrood, P. O. Box: 3619995161, Iran

    Shideh Mojerlou

  3. Department of Plant Pathology, Faculty of Agriculture, Tarbiat Modares University of Tehran, Tehran, Iran

    Naser Safaie

Authors
  1. Ferdos Ganji
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shideh Mojerlou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Naser Safaie
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Ferdos Ganji: investigation, visualization, writing — original draft Shideh Mojerlou: conceptualization, supervision, methodology, formal analysis, writing — review and editing Naser Safaie: conceptualization, supervision, methodology, data curation, writing — review and editing.

Corresponding author

Correspondence to Shideh Mojerlou.

Ethics declarations

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Robert Duran

Publisher's Note

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

Supplementary information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1381 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ganji, F., Mojerlou, S. & Safaie, N. Evaluation of copper-tolerant fungi isolated from Sarcheshmeh copper mine of Iran. Environ Sci Pollut Res 30, 110715–110724 (2023). https://doi.org/10.1007/s11356-023-30135-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-023-30135-1

Keywords

Search

Navigation