Skip to main content

Advertisement

SpringerLink
Log in

Fungi-assisted phytoextraction of lead: tolerance, plant growth–promoting activities and phytoavailability

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

Abstract

Lead (Pb) is known for its low mobility and persistence in soils. The main aim of the present study was to explore potential of different fungal strains to promote phytoextraction of Pb-contaminated soils. Five non-pathogenic fungal strains (Trichoderma harzianum, Penicillium simplicissimum, Aspergillus flavus, Aspergillus niger, and Mucor spp.) were tested for their ability to modify soil properties (pH and organic matter) and to increase Pb phytoavailability at varying concentrations. Lead tolerance of fungal strains followed the decreasing order as A. niger > T. harzianum > A. flavus > Mucor sp. > P. simplicissimum. Lead solubility induced by A. flavus and Mucor spp. was increased by 1.6- and 1.8-fold, respectively, as compared to the control soil (Pb added, without fungi). A. flavus and Mucor spp. lowered the soil pH by − 0.14 and − 0.13 units, in soils spiked with 2000 mg Pb kg−1. The maximum increase in the percentage of organic matter (OM) recorded was 1.7-fold for A. flavus at 500 mg Pb kg−1 soil. Plant growth–promoting assays confirmed the beneficial role of these fungal strains. Significantly high production of IAA (249 μg mL−1) and siderophores (61%) was observed with A. niger, and phosphate solubilization with P. simplicissimum (58 μg mL−1). Based on the results in Pb-contaminated soils, Pelargonium hortorum L. inoculated with Mucor spp. showed the potential to enhance phytoextraction of Pb by promoting Pb phytoavailability in soil and improving plant biomass production through plant growth–promoting activities.

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

Similar content being viewed by others

References

  • AFNOR (1994) Recueil de normes françaises. Qualité des sols, détermination du pH. AFNOR, Paris 63 pp

    Google Scholar 

  • Akhtar S, Iram S (2016) Enhanced phytoremediation of heavy metal polluted soil with native crops of Punjab, Pakistan. J Biodiver Env Sci 8(4):158–171

    Google Scholar 

  • Al-Askar AA (2016) Bioactive compounds produced by Trichoderma harzianum 1-SSR for controlling Fusarium verticillioides (Sacc.) Nirenberg and growth promotion of Sorghum vulgare. Egypt J Biol Pest Cont 26(2):379–386

    Google Scholar 

  • Al-Askar AA, Saber WIA, Ghoneem KM, Rashad YM (2018) Oxalic acid as the main molecule produced by Trichoderma asperellum MG323528 fermented on corn Stover based medium. Biotechnology 17(2):95–103

    Article  Google Scholar 

  • Arshad M, Silvestre J, Pinelli E, Kallerhoff J, Kaemmerer M, Tarigo A, Shahid M, Guiresse M, Pradère P, Dumat C (2008) A field study of lead phytoextraction by various scented Pelargonium cultivars. Chemosphere 71(11):2187–2192

    Article  CAS  Google Scholar 

  • Arshad M, Merlina G, Uzu G, Sobanska S, Sarret G, Dumat C, Silvestre J, Pinelli E, Kallerhoff J (2016) Phytoavailability of lead altered by two Pelargonium cultivars grown on contrasting lead-spiked soils. J Soils Sediments 16(2):581–591

    Article  CAS  Google Scholar 

  • Bhagobaty RK, Joshi SR (2009) Promotion of seed germination of green gram and chick pea by Penicillium verruculosum RS7PF, a root endophytic fungus of Potentilla fulgens L. J Adv Biotechnol 8(7):16–18

    Google Scholar 

  • Bilkay IS, Karakoç S, Aksöz N (2010) Indole-3-acetic acid and gibberellic acid production in Aspergillus niger. Turk J Biol 34:313–318

    CAS  Google Scholar 

  • Carson KC, Holliday S, Glenn AR, Dilworth MJ (1992) Siderophore and organic acid production in root nodule bacteria. Arch Microbiol 157(3):264–271

    Article  CAS  Google Scholar 

  • Chandran CS, Shijith KV, Vipin KV, Augusthy AR (2014) Study on heavy metals toxicity biomarkers in Aspergillus niger. Int J Adv Pharm Biol Chem 3(2):458–464

    CAS  Google Scholar 

  • Clesscerl LS, Greenberg AE, Eaton AD (1998) Standard Methods for the examination of water and wastewater, 20th edn. APHA-AWWA-WEF, Washington, DC

    Google Scholar 

  • Deng Z, Cao L, Huang H, Jiang X, Wang W, Shi Y, Zhang R (2011) Characterization of Cd-and Pb-resistant fungal endophyte Mucor sp. CBRF59 isolated from rapes (Brassica chinensis) in a metal-contaminated soil. J Hazard Mater 185(3):717–724

    Article  CAS  Google Scholar 

  • Gul I, Manzoor M, Hashim N, Yaqoob K, Kallerhoff J, Arshad M (2019a) Comparative effectiveness of organic and inorganic amendments on cadmium bioavailability and uptake by Pelargonium hortorum. J Soils Sediments. 19:2346–2356

    Article  CAS  Google Scholar 

  • Gul I, Manzoor M, Silvestre J, Rizwan M, Hina K, Kallerhoff J, Arshad M (2019b) EDTA-assisted phytoextraction of lead and cadmium by Pelargonium cultivars grown on spiked soil. Int J Phytorem 21:101–110

    Article  CAS  Google Scholar 

  • Hac-Wydro K, Sroka A, Jablo K (2016) The impact of auxins used in assisted phytoextraction of metals from the contaminated environment on the alterations caused by lead (II) ions in the organization of model lipid membranes. Colloids Surf B Biointerfaces 143:124–130

    Article  CAS  Google Scholar 

  • Hadi F, Bano A, Fuller MP (2010) The improved phytoextraction of lead (Pb) and the growth of maize (Zea mays L.): the role of plant growth regulators (GA3 and IAA) and EDTA alone and in combinations. Chemosphere 80(4):457–462

    Article  CAS  Google Scholar 

  • Hossain MM, Sultana F, Kubota M, Koyama H, Hyakumachi M (2007) The plant growth-promoting fungus Penicillium simplicissimum GP17-2 induces resistance in Arabidopsis thaliana by activation of multiple defense signals. Plant Cell Physiol 48(12):1724–1736

    Article  CAS  Google Scholar 

  • Iram S, Parveen K, Usman J, Nasir K, Akhtar N, Arouj S, Ahmad I (2012) Heavy metal tolerance of filamentous fungal strains isolated from soil irrigated with industrial wastewater. Biologija 58(3). https://doi.org/10.6001/biologija.v58i3.2527

  • 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):824–830

    Article  CAS  Google Scholar 

  • Kavamura VN, Esposito E (2010) Biotechnological strategies applied to the decontamination of soils polluted with heavy metals. Biotechnol Adv 28(1):61–69

    Article  CAS  Google Scholar 

  • López ML, Peralta-Videa JR, Benitez T, Gardea-Torresdey JL (2005) Enhancement of lead uptake by alfalfa (Medicago sativa) using EDTA and a plant growth promoter. Chemosphere 61(4):595–598

    Article  Google Scholar 

  • Manzoor M, Gul I, Silvestre J, Kallerhoff J, Arshad M (2018) Screening of indigenous ornamental species from different plant families for Pb accumulation potential exposed to metal gradient in spiked soils. Soil Sediment Contam 27(5):439–453

    Article  CAS  Google Scholar 

  • Manzoor M, Abid R, Rathinasabapathi B, De Oliveira LM, da Silva E, Deng F, Rensing C, Arshad M, Gul I, Xiang P, Ma LQ (2019a) Metal tolerance of arsenic–resistant bacteria and their ability to promote plant growth of Pteris vittata in Pb–contaminated soil. Sci Total Environ 660:18–24

    Article  CAS  Google Scholar 

  • Manzoor M, Gul I, Ahmed I, Zeeshan M, Hashmi I, Amin BAZ, Kallerhoff J, Arshad M (2019b) Metal tolerant bacteria enhanced phytoextraction of lead by two accumulator ornamental species. Chemosphere 227:561–569

    Article  CAS  Google Scholar 

  • Max B, Salgado JM, Rodríguez N, Cortés S, Converti A, Dominguez JM (2010) Biotechnological production of citric acid. Braz J Microbiol 41:862–875

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Munawar S, Iram S (2014) Chelating impact assessment of biological and chemical chelates on metal extraction from contaminated soils. J Chem Soc Pak 36(3):548–555

    CAS  Google Scholar 

  • Ousmanova D, Parker W (2007) Fungal generation of organic acids for removal of lead from contaminated soil. Water Air Soil Poll 179:65–380

    Article  Google Scholar 

  • Pikovskaya I (1948) Mobilization of phosphorus in soil connection with the vital activity of some microbial species. Microbiologia 17:362–370

    CAS  Google Scholar 

  • Povedano-Priego C, Martín-Sánchez I, Jroundi F, Sánchez-Castro I, Merroun ML (2017) Fungal biomineralization of lead phosphates on the surface of lead metal. Miner Eng 106:46–54

    Article  CAS  Google Scholar 

  • Prasad MNV, Freitas HMO (2003) Metal hyperaccumulation in plants - biodiversity prospecting for phytoremediation technology. Electron J Biotechnol 6(3):285–321

    Article  Google Scholar 

  • Ravanbakhsh M, Ronaghi AM, Taghavi SM, Jousset A (2016) Screening for the next generation heavy metal hyperaccumulators for dry land decontamination. J Environ Chem Eng 4(2):2350–2355

    Article  CAS  Google Scholar 

  • Reena T, Dhanya H, Deepthi MS, Pravitha DL (2013) Isolation of phosphate solubilizing bacteria and fungi from rhizospheres soil from banana plants and its effect on the growth of Amaranthus cruentus L. J Pharm Biol Sci 5(3):6–11

    Google Scholar 

  • Rizwan M, Ali S, Rehman MZ, Javed MR, Bashir A (2018) Lead toxicity in cereals and its management strategies: a critical review. Water Air Soil Pollut 229(211). https://doi.org/10.1007/s11270-018-3865-3

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  Google Scholar 

  • Shah GM, Tufail N, Bakhat HF, Ahmed I, Shahid M, Hammad HM, Nasim W, Rizwan M, Dong R (2019) Composting of municipal solid waste by different methods improved the growth of vegetables and reduced the health risks of cadmium and lead. Environ Sci Pollut Res 26:5463–5474

    Article  CAS  Google Scholar 

  • Smith E, Kempson IM, Juhasz AL, Weber J, Rofe A, Gancarz D, Naidu R, McLaren RG, Gräfe M (2011) In vivo–in vitro and XANES spectroscopy assessments of lead bioavailability in contaminated periurban soils. Environ Sci Technol 45(14):6145–6152

    Article  CAS  Google Scholar 

  • Usha S, Padmavathi T (2013) Effect of plant growth promoting microorganisms from rhizosphere of Piper nigrum L. Int J Pharm Bio Sci 4(1):835–846

    Google Scholar 

  • Velásquez L, Dussan J (2009) Biosorption and bioaccumulation of heavy metals on dead and living biomass of Bacillus sphaericus. J Hazard Mater 167(3):713–716

    Article  Google Scholar 

  • Wakelin SA, Warren RA, Harvey PR, Ryder MH (2004) Phosphate solubilization by Penicillium spp. closely associated with wheat roots. Biol Fert Soils 40(1):36–43

    Article  CAS  Google Scholar 

  • Walkley A, Black IA (1934) An examination of Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci 37:29–37

    Article  CAS  Google Scholar 

  • Xiao C, Chi R, He H, Qiu G, Wang D, Zhang W (2009) Isolation of phosphate-solubilizing fungi from phosphate mines and their effect on wheat seedling growth. Appl Biochem Biotech 159(2):330–342

    Article  CAS  Google Scholar 

  • Xiao C, Chi R, Li X, Xia M, Xia Z (2011) Biosolubilization of rock phosphate by three stress-tolerant fungal strains. Appl Biochem Biotech 165(2):719–727

    Article  CAS  Google Scholar 

  • Xu ZM, Tan XQ, Mei XQ, Li QS, Zhou C, Wang LL, Ye HJ, Yang P (2018) Low-Cd tomato cultivars (Solanum lycopersicum L.) screened in non-saline soils also accumulated low Cd, Zn, and Cu in heavy metal-polluted saline soils. Environ Sci Pollut Res 25(27):27439–27450

    Article  CAS  Google Scholar 

  • Yang Y, Han X, Liang Y, Ghosh A, Chen J, Tang M (2015) The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS ONE 10(12):e0145726. https://doi.org/10.1371/journal.pone.0145726

    Article  CAS  Google Scholar 

  • Yasser MM, Mousa ASM, Massoud ON, Nasr SH (2014) Solubilization of inorganic phosphate by phosphate solubilizing fungi isolated from Egyptian soils. J Biol Earth Sci 4(1):83–90

    Google Scholar 

  • Zhu SC, Tang JX, Zeng XX, Wei BJ, Huang B (2015) Isolation of Mucor circinelloides Z4 and Mucor racemosus Z8 from heavy metal-contaminated soil and their potential in promoting phytoextraction with Guizhou oilseed rap. J Central South Uni 22(1):88–94

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The work was part of Pak-France Collaborative Project PHC-PERIDOT jointly funded by HEC, Pakistan (no. 1-1/PERIDOT/R&D/HEC/2015) and Campus France (project no. 34362TM). The authors would like to acknowledge Fungal Culture Bank, University of Punjab, Lahore, Pakistan, for providing fungal strains for this study. The authors are also thankful to Dr. Maialen Barret, EcoLab, Toulouse, France, and Dr. Muhammad Faraz Bhatti, ASAB, NUST, Islamabad, Pakistan, for their guidance and support to carry out this study.

Author information

Authors and Affiliations

  1. Institute of Environmental Sciences and Engineering (IESE), School of Civil and Environmental Engineering (SCEE), National University of Sciences and Technology (NUST), Islamabad, Pakistan

    Maria Manzoor, Iram Gul & Muhammad Arshad

  2. Ecolab, Université de Toulouse, CNRS, Toulouse, France

    Jean Kallerhoff

Authors
  1. Maria Manzoor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Iram Gul
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean Kallerhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Muhammad Arshad
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Muhammad Arshad.

Additional information

Responsible editor: Elena Maestri

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 100 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Manzoor, M., Gul, I., Kallerhoff, J. et al. Fungi-assisted phytoextraction of lead: tolerance, plant growth–promoting activities and phytoavailability. Environ Sci Pollut Res 26, 23788–23797 (2019). https://doi.org/10.1007/s11356-019-05656-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-05656-3

Keywords

Search

Navigation