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.
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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
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
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
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
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
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
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
Buscaroli A (2017) An overview of indexes to evaluate terrestrial plants for phytoremediation purposes. Ecol Indic 82:367–380
Cambrollé J (2015) Evaluating wild grapevine tolerance to copper toxicity. Chemosphere 120:171–178
Cao X, Harris W (2010) Properties of dairy-manure-derived biochar pertinent to its potential use in remediation. Bioresour Technol 101:5222–5228
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
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
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
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
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
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
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
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
Eissa MA (2019) Effect of cow manure biochar on heavy metals uptake and translocation by zucchini (Cucurbita pepo L). Arab J Geosci 12:48
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
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
Ferreira DF (2011) Sisvar: a computer statistical analysis system. Ciência Agrotecnologia 35:1039–1042
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
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
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
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
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
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
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
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
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
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
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
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
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
Lamb DT, Naidu R, Ming H, Megharaj M (2012) Copper phytotoxicity in native and agronomical plant species. Ecotoxicol Environ Saf 85:23–29
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
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
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
Lichtenthaler HK, Miehé J (1997) Fluorescence imaging as a diagnostic tool for plant stress. Trends Plant Sci 2:316–320
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
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
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
McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opin Biotechnol 14:277–282
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
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998
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
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
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
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
Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401
Ramírez-Valdespino CA, Casas-Flores S, Olmedo-Monfil V (2019) Trichoderma as a model to study effector-like molecules. Front Microbiol 10:1030
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
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
Silva FC (2009) Manual de análises químicas de solos, plantas e fertilizantes, 2nd edn. Embrapa Informação Tecnológica, Brasília
Su C (2014) A review on heavy metal contamination in the soil worldwide: situation, impact and remediation techniques. Environ Skep Crit 3:24
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
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
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
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
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
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
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
Wiedmann TO, Schandl HMD (2015) The footprint of using metals: new metrics of consumption and productivity. Environ Econ Policy Stud 17:369–388
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
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
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
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
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
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
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
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
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.
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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
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DOI: https://doi.org/10.1007/s11368-019-02414-3