Skip to main content
Log in

Molecular identification and evaluation of gamma irradiation effect on modulating heavy metals tolerance in some of novel endophytic fungal strains

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Heavy metal (HM) pollution is a worldwide environmental issue. Given the urgent need to develop more powerful approaches for effective phytoremediation of HMs, isolation of novel endophytic strains from hyperaccumulator plants having potent HM tolerance is the main objective in this research. Moreover, the recovered strains were characterized and subjected to radiation mutagenesis to enhance their tolerance to HMs. Among 105 isolates, Alternaria alternata AUMC14431 was identified as the most effective Cd+2 tolerant strain having high recorded tolerance index (TI) (76.24%); in addition, the recorded minimum inhibitory concentration (MIC) was 300 ppm. Meanwhile, Chaetomium globosum AUMC14432 was identified as the most effective Pb+2 and Ni+2 tolerant strain having high recorded TI (97.46 and 93.34%, respectively); in addition, the evaluated MICs were 250 and 200 ppm, respectively. UV and gamma irradiation of the tested strains enhanced their Cd+2 and Pb+2 tolerance significantly (P ≤ 0.05). Meanwhile, irradiation had a negative impact on Ni+2 tolerance of C. globosum. The mutation incidence at the molecular level arising from exposure to irradiation was investigated. Genomic DNA of both the wild and mutated endophytic strains were isolated followed by random amplified polymorphic DNA (RAPD-PCR) analysis, using two short primers. A remarkable difference in DNA gel pattern between the wild type and mutated strains was observed. In conclusion, the novel isolated and irradiated endophytic strains, A. alternata S5 and C. globosum El26, having high efficiency in Cd+2 and Pb+2 tolerance, respectively, are considered to be prospective and powerful bioremediation candidates for potential application in microbially assisted phytoremediation.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abou Alhamed MF, Shebany YM (2012) Endophytic Chaetomium globosum enhances maize seedling copper stress tolerance. Plant Biol 14:859–863

    Article  CAS  Google Scholar 

  • Aishwarya S, Nagam N, Vijaya T, Netala RV (2017) Screening and identification of heavy metal-tolerant endophytic fungi Lasiodiplodia theobromae from Boswellia ovalifoliolata an endemic plant of tirumala hills. Asian J Pharm Clin Res 10:488–491

    Article  CAS  Google Scholar 

  • Alikamanoǧlu S (2002) Efficiency of the gamma irradiation in the induction of in vitro somatic mutations. J Cell Mol Biol 1(1)

  • Aly AH, Debbab A, Proksch P (2011) Fungal endophytes: unique plant inhabitants with great promises. Appl Microbiol Biotechnol 90:1829–1845. https://doi.org/10.1007/s00253-011-3270-y

    Article  CAS  PubMed  Google Scholar 

  • An H, Liu Y, Zhao X et al (2015) Characterization of Cadmium-resistant endophytic fungi from Salix variegata Franch. in Three Gorges Reservoir Region. China Microbiol Res 176:29–37. https://doi.org/10.1016/j.micres.2015.03.013

    Article  CAS  PubMed  Google Scholar 

  • Atienzar FA, Venier P, Jha AN, Depledge MH (2002) Evaluation of the random amplified polymorphic DNA (RAPD) assay for the detection of DNA damage and mutations. Mutat Res Toxicol Environ Mutagen 521:151–163

    Article  CAS  Google Scholar 

  • Choo J, Sabri NBM, Tan D et al (2015) Heavy metal resistant endophytic fungi isolated from Nypa fruticans in Kuching Wetland National Park. Ocean Sci J 50:445–453

    Article  CAS  Google Scholar 

  • Das D, Chakraborty A, Bhar S et al (2013) Gamma irradiation in modulating Cadmium bioremediation potential of Aspergillus sp. J Environ Sci Toxicol Food Technol 3:51–55

    Google Scholar 

  • Das D, Chakraborty A, Santra SC (2016) Ionising radiation in modulating zinc tolerance potential of Aspergillus niger. Proc Natl Acad Sci India Sect B Biol Sci 86:39–45. https://doi.org/10.1007/s40011-014-0397-5

    Article  CAS  Google Scholar 

  • Deng Z, Cao L (2017) Fungal endophytes and their interactions with plants in phytoremediation: a review. Chemosphere 168:1100–1106. https://doi.org/10.1016/j.chemosphere.2016.10.097

    Article  CAS  PubMed  Google Scholar 

  • Dong X, Li C, Li J et al (2010) A novel approach for soil contamination assessment from heavy metal pollution: a linkage between discharge and adsorption. J Hazard Mater 175:1022–1030

    Article  CAS  Google Scholar 

  • El-Sayed ER, Ahmed AS, Ismaiel AA (2019) Agro-industrial byproducts for production of the immunosuppressant mycophenolic acid by Penicillium roqueforti under solid-state fermentation: enhanced production by ultraviolet and gamma irradiation. Biocatal Agric Biotechnol. https://doi.org/10.1016/j.bcab.2019.01.053

    Article  Google Scholar 

  • El-Sayed ER, Ahmed AS, Abdelhakim HK (2020a) A novel source of the cardiac glycoside digoxin from the endophytic fungus Epicoccum nigrum: isolation, characterization, production enhancement by gamma irradiation mutagenesis and anticancer activity evaluation. J Appl Microbiol 128:747–762. https://doi.org/10.1111/jam.14510

    Article  CAS  PubMed  Google Scholar 

  • El-Sayed ER, Ahmed AS, Al-Hagar OEA (2020b) Agro-industrial wastes for production of paclitaxel by irradiated Aspergillus fumigatus under solid-state fermentation. J Appl Microbiol 128:1427–1439

    Article  CAS  Google Scholar 

  • El-Sayed ER, Ahmed AS, Hassan IA et al (2020c) Semi - continuous production of the anticancer drug taxol by Aspergillus fumigatus and Alternaria tenuissima immobilized in calcium alginate beads. Bioprocess Biosyst Eng 43:997–1008. https://doi.org/10.1007/s00449-020-02295-8

    Article  CAS  PubMed  Google Scholar 

  • El-Sayed ER, Zaki AG, Ahmed AS, Ismaiel AA (2020d) Production of the anticancer drug taxol by the endophytic fungus Epicoccum nigrum TXB502: enhanced production by gamma irradiation mutagenesis and immobilization technique. Appl Microbiol Biotechnol 104:6991–7003

    Article  CAS  Google Scholar 

  • Ezzouhri L, Castro E, Moya M et al (2009) Heavy metal tolerance of filamentous fungi isolated from polluted sites in Tangier, Morocco. African J Microbiol Res 3:35–48

    CAS  Google Scholar 

  • Fomina MA, Alexander IJ, Colpaert JV, Gadd GM (2005) Solubilization of toxic metal minerals and metal tolerance of mycorrhizal fungi. Soil Biol Biochem 37:851–866

    Article  CAS  Google Scholar 

  • Gontia-Mishra I, Tiwari S (2013) Molecular characterization and comparative phylogenetic analysis of phytases from fungi with their prospective applications. Food Technol Biotechnol 51:313–326

    CAS  Google Scholar 

  • Hemambika B, Rani MJ, Kannan VR (2011) Biosorption of heavy metals by immobilized and dead fungal cells: a comparative assessment. J Ecol Nat Environ 3:168–175

    CAS  Google Scholar 

  • Joshi BH (2014) Evaluation and characterization of heavy metal resistant fungi for their prospects in bioremediation. J Environ Res Dev 8:876–882

    Google Scholar 

  • Júnior FMRDS, Volcão LM, Hoscha LC, Pereira SV (2018) Growth of the fungus Chaetomium aureum in the presence of lead: implications in bioremediation. Environ Earth Sci 77:275

    Article  Google Scholar 

  • Khan AL, Waqas M, Hussain J et al (2015) Phytohormones enabled endophytic fungal symbiosis improve Aluminum phytoextraction in tolerant Solanum lycopersicum: an examples of Penicillium janthinellum LK5 and comparison with exogenous GA3. J Hazard Mater 295:70–78

    Article  CAS  Google Scholar 

  • Khan AR, Ullah I, Waqas M et al (2017) Host plant growth promotion and Cadmium detoxification in Solanum nigrum, mediated by endophytic fungi. Ecotoxicol Environ Saf 136:180–188

    Article  CAS  Google Scholar 

  • Li HY, Wei DQ, Shen M, Zhou ZP (2012) Endophytes and their role in phytoremediation. Fungal Divers 54:11–18. https://doi.org/10.1007/s13225-012-0165-x

    Article  Google Scholar 

  • Li L-S, Meng Y-P, Cao Q-F et al (2016a) Type 1 metallothionein (ZjMT) is responsible for heavy metal tolerance in Ziziphus jujuba. Biochem 81:565–573

    CAS  Google Scholar 

  • Li X, Li W, Chu L et al (2016b) Diversity and heavy metal tolerance of endophytic fungi from Dysphania ambrosioides, a hyperaccumulator from pb-Zn contaminated soils. J Plant Interact 11:186–192. https://doi.org/10.1080/17429145.2016.1266043

    Article  CAS  Google Scholar 

  • Ma Y, Oliveira RS, Nai F et al (2015) The hyperaccumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soil. J Environ Manage 156:62–69

    Article  CAS  Google Scholar 

  • Moubasher AH (1993) Soil fungi in Qatar and other Arab countries. University of Qatar, Doha, The Centre for Scientific and Applied Research

    Google Scholar 

  • Mousa SA, El-Sayed ER, Mohamed SS et al (2021) Novel mycosynthesis of Co3O4, CuO, Fe3O4, NiO, and ZnO nanoparticles by the endophytic Aspergillus terreus and evaluation of their antioxidant and antimicrobial activities. Appl Microbiol Biotechnol 105:741–753. https://doi.org/10.1007/s00253-020-11046-4

    Article  CAS  PubMed  Google Scholar 

  • Nandy S, Das T, Keeya C, Kumar D (2020) Fungal endophytes : Futuristic tool in recent research area of phytoremediation. South African J Bot in Press. https://doi.org/10.1016/j.sajb.2020.02.015

    Article  Google Scholar 

  • Nehnevajova E, Herzig R, Federer G et al (2005) Screening of sunflower cultivars for metal phytoextraction in a contaminated field prior to mutagenesis. Int J Phytoremediation 7:337–349

    Article  CAS  Google Scholar 

  • Oladipo OG, Olayinka A, Awotoye OO (2016) Maize (Zea mays L.) performance in organically amended mine site soils. J Environ Manage 181:435–442

    Article  CAS  Google Scholar 

  • Saiano F, Ciofalo M, Cacciola SO, Ramirez S (2005) Metal ion adsorption by Phomopsis sp. biomaterial in laboratory experiments and real wastewater treatments. Water Res 39:2273–2280

    Article  CAS  Google Scholar 

  • Saleem MY, Mukhtar Z, Cheema AA, Atta BM (2005) Induced mutation and in vitro techniques as a method to induce salt tolerance in Basmati rice (Oryza sauva L.). Int J Environ Sci Technol 2:141–145

    Article  CAS  Google Scholar 

  • Sardar K, Ali S, Hameed S et al (2013) Heavy metals contamination and what are the impacts on living organisms. Greener J Environ Manag Public Saf 2:172–179

    Article  Google Scholar 

  • Schulz B, Römmert A-K, Dammann U et al (1999) The endophyte-host interaction: a balanced antagonism? Mycol Res 103:1275–1283

    Article  Google Scholar 

  • Shen M, Liu L, Li D et al (2013) The effect of endophytic Peyronellaea from heavy metal-contaminated and uncontaminated sites on maize growth, heavy metal absorption and accumulation. Fungal Ecol 6:539–545. https://doi.org/10.1016/j.funeco.2013.08.001

    Article  Google Scholar 

  • Sianipar NF, Laurent D, Purnamaningsih R, Darwati I (2015) Genetic variation of the first generation of rodent tuber (Typhonium flagelliforme Lodd.) mutants based on RAPD molecular markers. HAYATI J Biosci 22:98–104

    Article  Google Scholar 

  • Siew C, Sim F, Tan WS et al (2016) Endophytes from Phragmites for metal removal: evaluating their metal tolerance, adaptive tolerance behaviour and biosorption efficacy tolerance, adaptive tolerance behaviour and biosorption efficacy. Desalin Water Treat 57:6959–6966. https://doi.org/10.1080/19443994.2015.1013507

    Article  CAS  Google Scholar 

  • Verma J, Bhatt A, Agrawal PK (2016) In-vitro study on bioaccumulation and tolerance of heavy metals by endophytic fungi Alternaria alternata isolated from Cupressus torulosa D.DON. Octa J Environ Res 4:146–154

    CAS  Google Scholar 

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

    Google Scholar 

  • Xiao X, Luo S, Zeng G et al (2010) Bioresource Technology Biosorption of Cadmium by endophytic fungus ( EF ) Microsphaeropsis sp. LSE10 isolated from Cadmium hyperaccumulator Solanum nigrum L. Bioresour Technol 101:1668–1674. https://doi.org/10.1016/j.biortech.2009.09.083

    Article  CAS  PubMed  Google Scholar 

  • Xu R, Li T, Cui H et al (2015) Diversity and characterization of Cd-tolerant dark septate endophytes ( DSEs ) associated with the roots of Nepal alder (Alnus nepalensis ) in a metal mine tailing of southwest China. Appl Soil Ecol 93:11–18. https://doi.org/10.1016/j.apsoil.2015.03.013

    Article  Google Scholar 

  • Xu J-Y, Han Y-H, Chen Y et al (2016) Arsenic transformation and plant growth promotion characteristics of As-resistant endophytic bacteria from As-hyperaccumulator Pteris vittata. Chemosphere 144:1233–1240

    Article  CAS  Google Scholar 

  • Yamaji K, Watanabe Y, Masuya H et al (2016) Root fungal endophytes enhance heavy- metal stress tolerance of Clethra barbinervis growing naturally at mining sites via growth enhancement promotion of nutrient uptake and decrease of heavy-metal concentration. PLoS ONE. https://doi.org/10.1371/journal.pone.0169089

    Article  PubMed  PubMed Central  Google Scholar 

  • Zaki AG, Ahmed AS, Mohamed GA et al (2014) Enhancement of gallic acid production by gamma irradiation of tannase-producing fungi. African J Biol Sci 376:1–12

    Google Scholar 

  • Zaki AG, El-shatoury EH, Ahmed AS, Al-hagar OEA (2019) Production and enhancement of the acetylcholinesterase inhibitor, huperzine A, from an endophytic Alternaria brassicae AGF041. Appl Microbiol Biotechnol 103:5867–5878. https://doi.org/10.1007/s00253-019-09897-7

    Article  CAS  PubMed  Google Scholar 

  • Zaki AG, El-Sayed ER, Elkodous MA, El-sayyad GS (2020a) Microbial acetylcholinesterase inhibitors for Alzheimer’s therapy: recent trends on extraction, detection, irradiation-assisted production improvement and nano-structured drug delivery. Appl Microbiol Biotechnol 104:4717–4735. https://doi.org/10.1007/s00253-020-10560-9

    Article  CAS  PubMed  Google Scholar 

  • Zaki AG, El-Shatoury EH, Ahmed AS, Al-Hagar OEA (2020b) Response surface methodology-mediated improvement of the irradiated endophytic fungal strain, Alternaria brassicae AGF041 for Huperzine A-hyperproduction. Lett Appl Microbiol 72:427–437. https://doi.org/10.1111/lam.13435

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to express their appreciation to Dr. Ali M. Saeed, lecturer at Microbiology Department, Faculty of Science, Ain Shams University for his assistance in Molecular identification part. Also, deep thanks to Dr. Gharieb S. El-Sayyad, Dr. Eman M. Kandeel, and Dr. Mokhtar K. Mohamed at the Egyptian Atomic Energy Authority (EAEA) for their continuous help. Special thanks to Mr. Ali M.A. Hessen, specialist at the Cyclotron unit, EAEA for his assistance in the gamma irradiation part.

Funding

Not applicable.

Author information

Authors and Affiliations

Authors

Contributions

YAH suggested the research point, investigated the article, conceived and designed the research, conducted experimental methodology, participated in data representation and manuscript writing, revising, and editing. AGZ conceived and designed the research, conducted experimental methodology, participated in data analysis and representation, wrote the original-draft, and participated in manuscript revising and editing. ASA conceived and designed research, provided the used chemicals, conducted experimental methodology, provided a practical guidance, and participated in manuscript revising and editing. GA conducted experimental methodology, participated in data analysis and representation, and participated in manuscript revising and editing. All authors read and approved the article.

Corresponding author

Correspondence to Amira G. Zaki.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals.

Additional information

Communicated by Erko Stackebrandt.

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 3001 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hasanien, Y.A., Zaki, A.G., Abdel-Razek, A.S. et al. Molecular identification and evaluation of gamma irradiation effect on modulating heavy metals tolerance in some of novel endophytic fungal strains. Arch Microbiol 203, 4867–4878 (2021). https://doi.org/10.1007/s00203-021-02472-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-021-02472-7

Keywords

Navigation