Skip to main content
Log in

A consortium of fungal isolates and biochar improved the phytoremediation potential of Jacaranda mimosifolia D. Don and reduced copper, manganese, and zinc leaching

  • Soils, Sec 2 • Global Change, Environ Risk Assess, Sustainable Land Use • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

A consortium of fungal isolates may improve phytoremediation by stimulating root growth whereas biochar reduces metal leaching in contaminated soils. We combined these treatments to evaluate to what extent Jacaranda mimosifolia D. Don seedlings extract metals (Cu, Mn, and Zn) and reduce leaching in soil columns.

Materials and methods

Contamination treatments were established by combining Cu (200 mg dm−3), Mn (450 mg dm−3), and Zn (450 mg dm−3). A spore suspension of five fungal isolates (Beauveria bassiana, Metarhizium anisopliae, Pochonia chlamydosporia, Purpureocillium lilacinum, and Trichoderma asperella) was sprayed on plant shoots and the soil surface. Biochar (1% m/v) was produced by the pyrolysis of wood sawdust and applied to the soil surface. Finally, control treatments were established in a completely randomized block design.

Results and discussion

The consortium of fungal isolates increased shoot and root mass, improved the translocation potential of Cu (translocation factor (TF) of 0.25), Mn (TF of 2.93), and Zn (TF of 1.79) from roots to shoots, and increased the total accumulated mass of Mn and Zn in shoots and roots. Biochar applications improved Cu, Mn, and Zn translocation and increased the total accumulated mass of shoot Mn. Moreover, a combination of fungal isolates and biochar increased the translocation factor to 0.44 for Cu, 1.70 for Mn, and 1.34 for Zn relative to the treatment with J. mimosifolia in contaminated soil (CJ); increased shoot Cu concentration; and reduced total leached Cu by a factor of 22.9, Mn by 5.5, and Zn by 22.9 relative to the CJ treatment. A photochemical profile, based on chlorophyll a fluorescence, showed that Jacaranda mimosifolia was tolerant to contaminated soil and is a potential phytoremediator of Cu, Mn, and Zn.

Conclusions

Overall, the consortium of fungal isolates and biochar improved the efficiency of phytoremediation by concentrating metals in plant tissue and reducing the risks of leaching.

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

Similar content being viewed by others

References

  • Ali A, Guo D, Zhang Y, Sun X, Jiang S, Guo Z, Huang H, Liang W, Li R, Zhang Z (2017) Using bamboo biochar with compost for the stabilization and phytotoxicity reduction of heavy metals in mine-contaminated soils of China. Sci Rep 7(1):1–12

    Google Scholar 

  • Ameh EG, Omatola OD, Akinde SB (2019) Phytoremediation of toxic metal polluted soil: screening for new indigenous accumulator and translocator plant species, northern Anambra Basin, Nigeria. Environ Earth Sci 78:345

    Google Scholar 

  • Ashraf S, Ali Q, Zahir ZA, Ashraf S, Asghar HN (2019) Phytoremediation: environmentally sustainable way for reclamation of heavy metal polluted soils. Ecotoxicol Environ Saf 174:714–727

    CAS  Google Scholar 

  • Bader AN, Salerno GL, Covacevich F et al (2019) Native Trichoderma harzianum strains from Argentina produce indole-3 acetic acid and phosphorus solubilization, promote growth and control wilt disease on tomato (Solanum lycopersicum L.). J King Saud Univ Sci. https://doi.org/10.1016/j.jksus.2019.04.002

    Google Scholar 

  • Bandara T, Herath I, Kumarathilaka P, Hseu ZY, Ok YS, Vithanage M (2017) Efficacy of woody biomass and biochar for alleviating heavy metal bioavailability in serpentine soil. Environ Geochem Health 39:391–401

    CAS  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S, Christensen RHB, Singmann H, Dai B, Scheipl F, Grothendieck G, Green P, Fox J (2018) Linear mixed-effects models using Eigen and S4. Package ‘Ime 4’. https://cran.r-project.org/web/packages/lme4/lme4.pdf. Accessed 14 January 2019

  • Bolhar-Nordenkampf H, Long S, Baker N, Oquist G, Schreiber U, Lechner E (1989) Chlorophyll fluorescence as a probe of the photosynthetic competence of leaves in the field: a review of current instrumentation. Funct Ecol 3:497–514

    Google Scholar 

  • Brotman Y, Lisec J, Méret M, Chet I, Willmitzer L, Viterbo A (2012) Transcript and metabolite analysis of the Trichoderma-induced systemic resistance response to Pseudomonas syringae in Arabidopsis thaliana. Microbiol 158:139–146

    CAS  Google Scholar 

  • Buscaroli A (2017) An overview of indexes to evaluate terrestrial plants for phytoremediation purposes. Ecol Indic 82:367–380

    CAS  Google Scholar 

  • Cambrollé J (2015) Evaluating wild grapevine tolerance to copper toxicity. Chemosphere 120:171–178

    Google Scholar 

  • Cao X, Harris W (2010) Properties of dairy-manure-derived biochar pertinent to its potential use in remediation. Bioresour Technol 101:5222–5228

    CAS  Google Scholar 

  • Cao L, Jiang M, Zeng Z, Du A, Tan H, Liu Y (2008) Trichoderma atroviride F6 improves phytoextraction efficiency of mustard (Brassica juncea (L.) Coss. var. foliosa Bailey) in Cd, Ni contaminated soils. Chemosphere 71:1769–1773

    CAS  Google Scholar 

  • Cavello IA, Crespo JM, García SS, Zapiola JM, Luna MF, Cavalitto SF (2015) Plant growth promotion activity of keratinolytic fungi growing on a recalcitrant waste known as “hair waste”. Biotechnol Res Int 2015:1–10. https://doi.org/10.1155/2015/952921

    Article  CAS  Google Scholar 

  • Chao Z, Yin-hua S, De-xin D et al (2019) Aspergillus niger changes the chemical form of uranium to decrease its biotoxicity, restricts its movement in plant and increase the growth of Syngonium podophyllum. Chemosphere 224:316–323

    CAS  Google Scholar 

  • Chen BC, Ho PC, Juang KW (2013) Alleviation effects of magnesium on copper toxicity and accumulation in grapevine roots evaluated with biotic ligand models. Ecotoxicol 22:174–183

    Google Scholar 

  • Chen Y, Yang W, Chao Y, Wang S, Tang YT, Qiu RL (2017) Metal-tolerant Enterobacter sp. strain EG16 enhanced phytoremediation using Hibiscus cannabinus via siderophore-mediated plant growth promotion under metal contamination. Plant Soil 413:203–216

    CAS  Google Scholar 

  • Conselho Nacional do Meio Ambiente - Conama. Resolução Conama n° 420, de 28 de dezembro de 2009. Brazilian Environmental Ministry. http://www.mma.gov.br/port/conama/res/res09/res42009.pdf. Accessed 04 July 2019

  • Contreras-Cornejo HA, Macías-Rodríguez L, Cortés-Penagos C, López-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol 149:1579–1592

    CAS  Google Scholar 

  • Contreras-Cornejo HA, Macías-Rodríguez L, Beltrán-Peña E, Herrera-Estrella A, López-Bucio J (2011) Trichoderma-induced plant immunity likely involves both hormonal-and camalexin-dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungi Botrytis cinerea. Plant Signal Behav 6:1554–1563

    CAS  Google Scholar 

  • Dube A, Zbytniewski R, Kowalkowski T, Cukrowska E, Buszewski B (2001) Adsorption and migration of heavy metals in soil. Pol J Environ Stud 10:1–10

    CAS  Google Scholar 

  • Eissa MA (2019) Effect of cow manure biochar on heavy metals uptake and translocation by zucchini (Cucurbita pepo L). Arab J Geosci 12:48

    Google Scholar 

  • Farias CP, Carvalho RC, Resende FL, Azevedo LCB (2018) Consortium of five fungal isolates conditioning root growth and arbuscular mycorrhiza in soybean, corn, and sugarcane. Ann Acad Bras Cienc 90:3649–3660

    CAS  Google Scholar 

  • Feng NX, Yu J, Zhao HM, Cheng YT, Mo CH, Cai QY, Li YW, Li H, Wong MH (2017) Efficient phytoremediation of organic contaminants in soils using plant–endophyte partnerships. Sci Total Environ 583:352–368

    CAS  Google Scholar 

  • Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciência Agrotecnologia 35:1039–1042

    Google Scholar 

  • Fox J, Weisberg S, Adler D, Bates D, Baud-Bovy G, Ellison S et al (2015) Companion to applied regression. Package ‘car’. URL https://CRAN.R-project.org/package=car. R package version. Accessed 15 March 2018

  • Gibson DM, Donzelli BG, Krasnoff SB, Keyhani NO (2014) Discovering the secondary metabolite potential encoded within entomopathogenic fungi. Nat Prod Rep 31:1287–1305

    CAS  Google Scholar 

  • Gong X, Huang D, Liu Y, Zeng G, Chen S, Wang R, Xu P, Cheng M, Zhang C, Xue W (2019a) Biochar facilitated the phytoremediation of cadmium contaminated sediments: metal behavior, plant toxicity, and microbial activity. Sci Total Environ 666:1126–1133

    CAS  Google Scholar 

  • Gong Q, Wang L, Dai T, Zhou J, Kang Q, Chen H, Li K, Li Z (2019b) Effects of copper on the growth, antioxidant enzymes and photosynthesis of spinach seedlings. Ecotoxicol Environ Saf 171:771–780

    CAS  Google Scholar 

  • Hermosa R, Rubio MB, Cardoza RE, Nicolás C, Monte E, Gutiérrez S (2013) The contribution of Trichoderma to balancing the costs of plant growth and defense. Int Microbiol 16:69–80

    CAS  Google Scholar 

  • Husson F et al (2017) FactoMineR: multivariate exploratory data analysis and data mining. Package ‘FactoMineR’. https://cran.r-project.org/web/packages/FactoMineR/index.html. Accessed 15 March 2018

  • Jaber LR, Enkerli J (2016) Effect of seed treatment duration on growth and colonization of Vicia faba by endophytic Beauveria bassiana and Metarhizium brunneum. Biol Control 103:187–195

    CAS  Google Scholar 

  • Janik E, Maksymiec W, Gruszecki WI (2010) The photoprotective mechanisms in Secale cereale leaves under Cu and high light stress condition. J Photochem Photobiol 101:47–52

    CAS  Google Scholar 

  • Kargar M, Clark OG, Hendershot WH, Jutras P, Prasher SO (2015) Immobilization of trace metals in contaminated urban soil amended with compost and biochar. Water Air Soil Pollut 226:191

    Google Scholar 

  • Khalid S, Shahid M, Niazi NK, Murtaza B, Bibi I, Dumat C (2017) A comparison of technologies for remediation of heavy metal contaminated soils. J Geochem Explor 182:247–268

    CAS  Google Scholar 

  • Khan MR, Mohiddin FA, Ejaz MN, Khan MM (2012) Management of root-knot disease in eggplant through the application of biocontrol fungi and dry neem leaves. Turk J Biol 36:161–169

    Google Scholar 

  • Khan Y, Ali B, Cui X, Feng Y, Yang X, Stoffella PJ (2017) Impact of different feedstocks derived biochar amendment with cadmium low uptake affinity cultivar of pak choi (Brassica rapa ssb. chinensis L.) on phytoavoidation of Cd to reduce potential dietary toxicity. Ecotoxicol Environ Saf 141:129–138

    CAS  Google Scholar 

  • Kim HS, Kim KR, Kim HJ, Yoon JH, Yang JE, Ok YS, Owens G, Kim KH (2015) Effect of biochar on heavy metal immobilization and uptake by lettuce (Lactuca sativa L.) in agricultural soil. Environ Earth Sci 74:1249–1259

    CAS  Google Scholar 

  • Lam EJ, Cánovas M, Gálvez ME, Montofré ÍL, Keith BF, Faz Á (2017) Evaluation of the phytoremediation potential of native plants growing on a copper mine tailing in northern Chile. J Geochem Explor 182:210–217

    CAS  Google Scholar 

  • Lam EJ, Gálvez ME, Cánovas M, Montofré ÍL, Keith BF (2018) Assessment of the adaptive capacity of plant species in copper mine tailings in arid and semiarid environments. J Soils Sediments 18:2203–2216

    CAS  Google Scholar 

  • Lamb DT, Naidu R, Ming H, Megharaj M (2012) Copper phytotoxicity in native and agronomical plant species. Ecotoxicol Environ Saf 85:23–29

    CAS  Google Scholar 

  • Li X, Zhang X, Wang X, Yang X, Cui Z (2019) Bioaugmentation-assisted phytoremediation of lead and salinity co-contaminated soil by Suaeda salsa and Trichoderma asperellum. Chemosphere 224:716–725

    CAS  Google Scholar 

  • Liao X, Lu HL, Fang W, Leger RJS (2014) Overexpression of a Metarhizium robertsii HSP25 gene increases thermotolerance and survival in soil. Appl Microbiol Biotechnol 98:777–783

    CAS  Google Scholar 

  • Liao X, Lovett B, Fang W, St Leger RJ (2017) Metarhizium robertsii produces indole-3-acetic acid, which promotes root growth in Arabidopsis and enhances virulence to insects. Microbiol 163:980–991

    CAS  Google Scholar 

  • Lichtenthaler HK, Miehé J (1997) Fluorescence imaging as a diagnostic tool for plant stress. Trends Plant Sci 2:316–320

    Google Scholar 

  • Ma Y, Zhang C, Oliveira RS, Freitas H, Luo Y (2016) Bioaugmentation with endophytic bacterium E6S homologous to Achromobacter piechaudii enhances metal rhizoaccumulation in host Sedum plumbizincicola. Front Plant Sci 7:75

    Google Scholar 

  • Martínez-Medina A, Roldán A, Albacete A, Pascual JA (2011) The interaction with arbuscular mycorrhizal fungi or Trichoderma harzianum alters the shoot hormonal profile in melon plants. Phytochem 72:223–229

    Google Scholar 

  • Martínez-Medina A, Alguacil MDM, Pascual JA, Van Wees SC (2014) Phytohormone profiles induced by Trichoderma isolates correspond with their biocontrol and plant growth-promoting activity on melon plants. J Chem Ecol 40:804–815

    Google Scholar 

  • McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282

    CAS  Google Scholar 

  • Mishra J, Singh R, Arora NK (2017) Alleviation of heavy metal stress in plants and remediation of soil by rhizosphere microorganisms. Front Microbiol 8:1706

    Google Scholar 

  • Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998

    CAS  Google Scholar 

  • Oggerin M, Tornos F, Rodríguez N, Del Moral C, Sánchez-Román M, Amils R (2013) Specific jarosite biomineralization by Purpureocillium lilacinum, an acidophilic fungi isolated from Río Tinto. Environ Microbiol 15:2228–2237

    CAS  Google Scholar 

  • Oh TK, Choi B, Shinogi Y, Chikushi J (2012) Effect of pH conditions on actual and apparent fluoride adsorption by biochar in aqueous phase. Water Air Soil Pollut 223:3729–3738

    CAS  Google Scholar 

  • Oliveira DC, Moreira ASF, Isaias RMV, Rezende UC (2017) Sink status and photosynthetic rate of the leaflet galls induced by Bystracoccus mataybae (Eriococcidae) on Matayba guianensis (Sapindaceae). Front Plant Sci 8:1249

    Google Scholar 

  • Prakongkep N, Gilkes RJ, Wiriyakitnateekul W (2015) Forms and solubility of plant nutrient elements in tropical plant waste biochars. J Plant Nutr Soil Sci 178:732–740

    CAS  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    CAS  Google Scholar 

  • Ramírez-Valdespino CA, Casas-Flores S, Olmedo-Monfil V (2019) Trichoderma as a model to study effector-like molecules. Front Microbiol 10:1030

    Google Scholar 

  • R Development Core Team (2017) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Sasan RK, Bidochka MJ (2012) The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. Am J Bot 99:101–107

    Google Scholar 

  • Shi Y, Xie H, Cao L, Zhang R, Xu Z, Wang Z, Deng Z (2017) Effects of Cd- and Pb-resistant endophytic fungi on growth and phytoextraction of Brassica napus in metal-contaminated soils. Environ Sci Pollut Res 24:417–426

    CAS  Google Scholar 

  • Silva FC (2009) Manual de análises químicas de solos, plantas e fertilizantes, 2nd edn. Embrapa Informação Tecnológica, Brasília

    Google Scholar 

  • Su C (2014) A review on heavy metal contamination in the soil worldwide: situation, impact and remediation techniques. Environ Skep Crit 3:24

    Google Scholar 

  • Sun X, Li B, Han F, Xiao E, Xiao T, Sun W (2019) Impacts of arsenic and antimony co-contamination on sedimentary microbial communities in rivers with different pollution gradients. Microb Ecol. https://doi.org/10.1007/s00248-019-01327-5

    CAS  Google Scholar 

  • Thakur S, Singh L, Ab Wahid Z, Siddiqui MF, Atnaw SM, Din MFM (2016) Plant-driven removal of heavy metals from soil: uptake, translocation, tolerance mechanism, challenges, and future perspectives. Environ Monit Assess 188:206

    Google Scholar 

  • Uchimiya M, Lima IM, Klasson KT, Wartelle LH (2010) Contaminant immobilization and nutrient release by biochar soil amendment: roles of natural organic matter. Chemosphere 80:935–940

    CAS  Google Scholar 

  • Vaillant N, Monnet F, Hitmi A, Sallanon H, Coudret A (2005) Comparative study of responses in four Datura species to a zinc stress. Chemosphere 59:1005–1013

    CAS  Google Scholar 

  • Vinayarani G, Madhusudhan KN, Prakash HS (2019) Induction of systemic resistance in turmeric by rhizospheric isolate Trichoderma asperellum against rhizome rot disease. J Plant Pathol. https://doi.org/10.1007/s42161-019-00303-9

    Google Scholar 

  • Wang D, Li C, Parikh SJ, Scow KM (2019a) Impact of biochar on water retention of two agricultural soils–a multi-scale analysis. Geoderma 340:185–191

    CAS  Google Scholar 

  • Wang M, Ren L, Wang D, Cai Z, Xia X, Ding A (2019b) Assessing the capacity of biochar to stabilize copper and lead in contaminated sediments using chemical and extraction methods. J Environ Sci 79:91–99

    Google Scholar 

  • Wiedmann TO, Schandl HMD (2015) The footprint of using metals: new metrics of consumption and productivity. Environ Econ Policy Stud 17:369–388

    Google Scholar 

  • Wuana RA, OKieimen FE (2011, 2011) Heavy metals in contaminated soils: a review of sources, chemistry, risks and best available strategies for remediation. Int Sch Res Notices:1–20. https://doi.org/10.5402/2011/402647

    Google Scholar 

  • Yang X (2018) Principles and technologies of phytoremediation for metal-contaminated soils: a review. In: Luo Y, Tu C (eds) Twenty years of research and development on soil pollution and remediation in China. Springer, Singapore, pp 279–331

    Google Scholar 

  • Yoon J, Cao X, Zhou Q, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464

    CAS  Google Scholar 

  • Zavala-Gonzalez EA, Escudero N, Lopez-Moya F, Aranda-Martinez A, Exposito A, Ricaño-Rodríguez J, Naranjo-Ortiz MA, Ramírez-Lepe M, Lopez-Llorca LV (2015) Some isolates of the nematophagous fungus Pochonia chlamydosporia promote root growth and reduce flowering time of tomato. Ann Appl Biol 166:472–483

    CAS  Google Scholar 

  • Zhang X, Wang H, He L, Lu K, Sarmah A, Li J, Huang H (2013) Using biochar for remediation of soils contaminated with heavy metals and organic pollutants. Environ Sci Pollut Res 20:8472–8483

    CAS  Google Scholar 

  • Zhang S, Gan Y, Xu B (2019) Mechanisms of the IAA and ACC-deaminase producing strain of Trichoderma longibrachiatum T6 in enhancing wheat seedling tolerance to NaCl stress. BMC Plant Biol 19:22

    CAS  Google Scholar 

  • Zhao T, Zhang K, Chen J, Shi X, Li X, Ma Y, Fang G, Xu S (2019) Changes in heavy metal mobility and availability in contaminated wet-land soil remediated using lignin-based poly (acrylic acid). J Hazard Mater 368:459–467

    CAS  Google Scholar 

  • Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer-Verlag, New York. https://doi.org/10.1007/978-0-387-87458-6

    Book  Google Scholar 

Download references

Acknowledgments

Authors thank the reviewers for their comments and suggestions for improving this manuscript. We are grateful to Biosag - Comércio e Serviços Agrícolas Ltda and to Msc. The authors are grateful to the City Hall of Uberlândia for providing J. mimosifolia seedlings, and to João C.F. Cardoso who helped us with the PCA and the multivariate linear mixed model analysis of the photosynthesis data.

Funding

This study was funded by Biosag - Comércio e Serviços Agrícolas Ltda (ICIAG.PEQU.0037). CPF received a mastering course scholarship grant from Biosag - Comércio e Serviços Agrícolas Ltda. LCBA received a scholarship grant from Biosag.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lucas Carvalho Basilio Azevedo.

Ethics declarations

All authors attest consent for publishing. The research project has been submitted and approved at Council of Institute of Agricultural Sciences and by the Pro-Rectory of Research and Post-Graduation Studies of Federal University of Uberlândia.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Hailong Wang

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

Farias, C.P., Alves, G.S., Oliveira, D.C. et al. A consortium of fungal isolates and biochar improved the phytoremediation potential of Jacaranda mimosifolia D. Don and reduced copper, manganese, and zinc leaching. J Soils Sediments 20, 260–271 (2020). https://doi.org/10.1007/s11368-019-02414-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-019-02414-3

Keywords

Navigation