Trichoderma tomentosum Ts141 as a Potential Candidate for Bioremediation of Cadmium, Lead, and Nickel Ions

Document Type : Original Research Paper

Authors

1 Department of Microbiology, Faculty of Biological Sciences, Alzahra University, Tehran, Iran

2 Department of Production Engineering and Plant Genetics, Faculty of Agriculture, University of Maragheh, Iran, P.O. Box 55181-83111, Iran

3 Department of Biology, Faculty of Science, University of Maragheh, Maragheh, Iran P.O. Box 55181-83111, Iran

Abstract

Fungi are successful microorganisms in the bioremediation of environmental pollution. So, this study aimed to determine the potential of Trichoderma tomentosum to remediate cadmium, lead, and nickel contaminations from potato dextrose agar (PDA) and potato dextrose broth (PDB) media. Growth rates, toxicity tolerance sporulation, bio-sorption capacity, and bio-sorption efficiency of the fungus were evaluated under different concentrations of CdCl2, Pb(NO3)2, and NiCl2. The findings demonstrated that the growth rate of the fungus differed depending on concentration, metal type, and medium. More metals in PDA medium induced more inhibition on fungus growth rates; however, the rate was independent from the heavy metals concentrations in PDB medium. Cadmium was the most toxic metal tested against T. tomentosum, with a 72h LC50 of 37 ppm. It was about 3.16 and 4.24 times as toxic as nickel and lead, respectively. In the control condition, sporulation of the fungus began at 72 hours, but under the heavy metals, it began at 168, 168, and 192 hours, respectively, for Pb, Ni, and Cd. Both the bio-sorption capacity and efficacy of the fungus were significantly enhanced by an increase in metal content and the highest values were obtained at 200 ppm of the salts. The heavy metals total bio-sorption capacity order was Ni < Cd < Pb in the aqueous medium. The conclusion was that T. tomentosum has a greater potential for the biosorption of heavy metals; hence, the fungus may be employed for the bioremediation of heavy metals from polluted sites, particularly wastewater and industrial influents. 

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Afshin, S., Rashtbari, Y., Vosough, M., Dargahi, A., Fazlzadeh, M., Behzad, A. & Yousefi, M. (2021). Application of Box–Behnken design for optimizing parameters of hexavalent chromium removal from aqueous solutions using Fe3O4 loaded on activated carbon prepared from alga: kinetics & equilibrium study. JWPE, 42;102113.
Alengebawy, A., Abdelkhalek, S.T., Qureshi, S.R. & Wang, M.Q. (2021). Heavy metals & pesticides toxicity in agricultural soil & plants: Ecological risks & human health implications. Toxics, 9(3);42.
Anahid, S., Yaghmaei, S. & Ghobadinejad, Z. (2011). Heavy metal tolerance of fungi. Sci. Iran., 18(3);502-508.
Azevedo, M.M. & Cássio, F. (2010). Effects of metals on growth & sporulation of aquatic fungi. Drug Chem. Toxicol., 33(3);269-278.
Chew, A.W., Rahman, N.N., Kadir, M.O. & Chen, C.C. (2012), Dried & wet Trichoderma sp, biomass adsorption capacity on Ni, Cd & Cr in contaminated groundwater, IPCBEE, 10-11.
Dehghani, M.H., Tajik, S., Panahi, A., Khezri, M., Zarei, A., Heidarinejad, Z. & Yousefi, M. (2018). Adsorptive removal of noxious cadmium from aqueous solutions using poly urea-formaldehyde: a novel polymer adsorbent. MethodsX, 5;1148-1155.
Dixit, P., Mukherjee, P.K., Sherkhane, P.D., Kale, S.P. & Eapen, S. (2011), Enhanced tolerance & remediation of anthracene by transgenic tobacco plants expressing a fungal glutathione transferase gene, J. Hazard. Mater., 192(1);270-276.
Dugal, S. & Gangawane, M. (2012). Metal tolerance & potential of penicillium species for use in mycoremediation. Int. J. Chem. Pharm. Res., 4(5);2362-2366.
Ezeonuegbu, B.A., Machido, D.A. & Yakubu, S.E. (2015), Capacity of fungal genera isolated from refinery effluents to remove & bioaccumulate lead, nickel & cadmium from refinery waste, Int. j. sci. technol., 3(6);47.
Faedda, R., Puglisi, I., Sanzaro, V., Petrone, G. & Cacciola, S.O. (2012), Expression of genes of Trichoderma harzianum in response to the presence of cadmium in the substrate, Nat. Prod. Res., 26(24);2301-2308,
Fargasova, A. (2004). Toxicity comparison of some possible toxic metals (Cd, Cu, Pb, Se, Zn) on young seedlings of Sinapis alba L. Plant, Soil Environ., 50(1);33-38.
Fu, K., Fan, L., Li, Y., Gao, S. & Chen, J. (2012), Tmac1, a transcription factor which regulated high affinity copper transport in Trichoderma reesei, Microbiol. Res., 167(9);536-543.
Gonzalez-Guerrero, M., Melville, L.H., Ferrol, N., Lott, J.N., Azcon-Aguilar, C. & Peterson, R.L. (2008), Ultrastructural localization of heavy metals in the extraradical mycelium & spores of the arbuscular mycorrhizal fungus Glomus intraradices, Can. J. Microbiol., 54(2);103-110.
Idris, M. O., Yaqoob, A. A., Ibrahim, M. N. M., Ahmad, A., & Alshammari, M. B. (2023). Introduction of adsorption techniques for heavy metals remediation. In Emerging Techniques for Treatment of Toxic Metals from Wastewater (pp. 1-18). Elsevier.
Iram, S., Shabbir, R., Zafar, H. & Javaid, M. (2015). Biosorption & bioaccumulation of copper & lead by heavy metal-resistant fungal isolates. Arabian J. Sci. Eng., 40(7);1867-1873.
Iskandar, N.L., Zainudin, N.A.I.M., & Tan, S.G. (2011). Tolerance & biosorption of copper (Cu) & lead (Pb) by filamentous fungi isolated from a freshwater ecosystem. Res. J. Environ. Sci., 23(5);824-830.
Kacprzak, M.J., Rosikon, K., Fijalkowski, K., & Grobelak, A. (2014), The effect of Trichoderma on heavy metal mobility & uptake by Miscanthus giganteus, Salix sp, Phalaris arundinacea, & Panicum virgatum, Appl. Environ. Soil Sci.
Kaur, S., Midha, T., Verma, H., Muduli, R. R., Dutta, O., Saini, O., ... & Dhiman, M. (2023). Bioremediation: A favorable perspective to eliminate heavy metals from polluted soil. In Metagenomics to Bioremediation (pp. 209-230). Academic Press.
Khan, R.A.A., Najeeb, S., Hussain, S., Xie, B., & Li, Y. (2020). Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic fungi. Microorganisms, 8(6);817.
Kumar, R., Bhatia, D., Singh, R., Rani, S., & Bishnoi, N. R., (2011), Sorption of heavy metals from electroplating effluent using immobilized biomass Trichoderma viride in a continuous packed-bed column, Int. Biodeterior. Biodegrad., 65(8);1133-1139.
Kumar, Y.P., King, P. & Prasad, V.S.R.K. (2006). Equilibrium & kinetic studies for the biosorption system of copper (II) ion from aqueous solution using Tectona grandis Lf leaves powder. J. Hazard. Mater., 137(2);1211-1217.
Kumara, R.R., Leeb, J.T. & Chob, J.Y. (2012), Toxic cadmium ions removal by isolated fungal strain from e-waste recycling facility, J. Environ. Health Sci. Eng., 23(19);8745.
Lin, H., Wang, Z., Liu, C., & Dong, Y. (2022). Technologies for removing heavy metal from contaminated soils on farmland: A review. Chemosphere, 305;135457.
Liu, S.H., Zeng, G.M., Niu, Q.Y., Liu, Y., Zhou, L., Jiang, L.H., Tan, X.F., Xu, P., Zhang, C. & Cheng, M. (2017). Bioremediation mechanisms of combined pollution of PAHs & heavy metals by bacteria & fungi: A mini review. Bioresour. Technol., 224;25-33.
Malkoc, S., Kurt, H., Ozbayer, C. & Yagci, E. (2021). Mycoremediation of Trichoderma harzianum & Penicillium chrysogenum to Pb Exposure: Effect on Metal Bioaccumulation, Oxidative Stress & Antioxidant System. CRPASE, 7(2);1-4.
Mohammadi, A.A., Yousefi, M., Soltani, J., Ahangar, A.G. & Javan, S. (2018). Using the combined model of gamma test & neuro-fuzzy system for modeling & estimating lead bonds in reservoir sediments. ESPR, 25(30);30315-30324.
Mohsenzadeh, F. & Shahrokhi, F. (2014). Biological removing of Cadmium from contaminated media by fungal biomass of Trichoderma species. J. Environ. Health Sci. Eng., 12(1);1-7.
Mohsenzadeh, F., Chehregani Rad, A. & Akbari, M. (2012), Evaluation of oil removal efficiency & enzymatic activity in some fungal strains for bioremediation of petroleum-polluted soils, Iran. J. Environ. Health Sci. Eng., 9(1);1-8.
Mohsenzadeh, F., Nasseri, S., Mesdaghinia, A., Nabizadeh, R., Zafari, D., Khodakaramian, G. & Chehregani, A. (2010), Phytoremediation of petroleum-polluted soils: Application of Polygonum aviculare & its root-associated (penetrated) fungal strains for bioremediation of petroleum-polluted soils, Ecotoxicol. Environ. Saf., 73(4);613-619.
Nagajyoti, P. C., Lee, K. D., & Sreekanth, T.V.M. (2010), Heavy metals, occurrence & toxicity for plants: a review, Environ. Chem. Lett., 8(3);199-216.
Puglisi, I., Faedda, R., Sanzaro, V., Piero, A.R.L., Petrone,G. & Cacciola, S.O. (2012), Identification of differentially expressed genes in response to mercury I & II stress in Trichoderma harzianum, Gene., 506(2);325-330.
Rao, M.A., Scelza, R., Scotti, R. & Gianfreda, L. (2010). Role of enzymes in the remediation of polluted environments. J. Soil Sci. Plant Nutr., 10(3);333-353.
Sahu, A., Mandal, A., Thakur, J., Manna, M.C. & Rao, A.S. (2012). Exploring bioaccumulation efficacy of Trichoderma viride: an alternative bioremediation of cadmium & lead. Natl. Acad. Sci. Lett. (India), 35(4);299-302.
Selen, V. Özer, D. & Özer, A. (2014). A study on the removal of Cr (VI) ions by sesame (Sesamum indicum) stems dehydrated with sulfuric acid. Arabian J. Sci. Eng., 39(8);5895-5904.
Sharma, S.S., Dietz, K.J. & Mimura, T. (2016). Vacuolar compartmentalization as indispensable component of heavy metal detoxification in plants. Plant, Cell Environ., 39(5);1112-1126.
Shi, C., He, H., Xia, Z., Gan, H., Xue, Q., Cui, Z. & Chen, J. (2022). Heavy metals & Pb isotopes in a marine sediment core record environmental changes & anthropogenic activities in the Pearl River Delta over a century. Sci. Total Environ., 814;151934.
Shoaib, A., Naureen, A., Tanveer, F. & Aslam, N. (2012), Removal of Ni (II) Ions from Substrate using Filamentous Fungi, Int. J. Agric. Biol., 14(5).
Shokri, S., Abdoli, N., Sadighara, P., Mahvi, A.H., Esrafili, A., Gholami, M., Jannat, B. & Yousefi, M. (2022). Risk assessment of heavy metals consumption through onion on human health in Iran. Food Chemistry.,14;100283.
Siddiquee, S., Aishah, S.N., Azad, S.A., Shafawati, S.N. & Naher, L. (2013). Tolerance & biosorption capacity of Zn2+, Pb2+, Ni 3+ & Cu2+ by filamentous fungi (Trichoderma harzianum, T. aureoviride & T. virens), SCIRP.,4(4);1-14
Singh, G., Nema, R., Khare, S., Singh, D., Jain, P., Pradhan, A., Gupta, A. & Naidu, S. (2012), Tolerance & biodegradation capacity of Trichoderma viride with special reference to heavy metals (Cr, Cd), Indo Am. J. Pharm. Res., 2(10);1007-1014.
Sytar, O., Kumar, A., Latowski, D., Kuczynska, P., Strzałka, K. & Prasad, M.N.V. (2013), Heavy metal-induced oxidative damage, defense reactions, & detoxification mechanisms in plants, Acta Physiol. Plant., 35(4);985-999.
Teng, Y., Luo, Y., Ma, W., Zhu, L., Ren, W., Luo, Y., Christie, P. & Li, Z. (2015), Trichoderma reesei FS10-C enhances phytoremediation of Cd-contaminated soil by Sedum plumbizincicola & associated soil microbial activities, Front. Plant Sci., 9;220.
Tripathi, P., Singh, P.C., Mishra, A., Chauhan, P.S., Dwivedi, S., Bais, R.T. & Tripathi, R.D. (2013), Trichoderma: a potential bioremediator for environmental clean up, Clean Technol. Environ. Policy., 15(4);541-550.
Tyśkiewicz, R., Nowak, A., Ozimek, E., & Jaroszuk-Ściseł, J. (2022). Trichoderma: The current status of its application in agriculture for the biocontrol of fungal phytopathogens & stimulation of plant growth. Int. J. Mol. Sci., 23(4), 2329.
Valix, M. & Loon, L.O. (2003). Adaptive tolerance behaviour of fungi in heavy metals. Miner. Eng., 16(3);193-198.
Verena, S.S., Alfredo, H.E., Enrique, M. & Susanne, Z. (2011). Trichoderma: the genomics of opportunistic success. Nat. Rev. Microbiol., 9(10).
Wang, B. & Wang, K. (2013). Removal of copper from acid wastewater of bioleaching by adsorption onto ramie residue & uptake by Trichoderma viride. Bioresour. Technol., 136;244-250.
Xu, P., Zeng, G., Huang, D., Liu, L., Zhao, M., Lai, C., Li, N., Wei, Z., Huang, C. & Zhang, C. (2016), Metal bioaccumulation, oxidative stress & antioxidant defenses in Phanerochaete chrysosporium response to Cd exposure, Ecol. Eng., 87;150-156.
Yaashikaa, P.R., Kumar, P.S., Jeevanantham, S. & Saravanan, R. (2022). A review on bioremediation approach for heavy metal detoxification & accumulation in plants. Environ. Pollut., 119035.
Yadav, S.K. (2010). Heavy metals toxicity in plants: an overview on the role of glutathione & phytochelatins in heavy metal stress tolerance of plants. S. Afr. J. Bot., 76(2);167-179.
Yang, X., Feng, Y., He, Z. & Stoffella, P.J. (2005). Molecular mechanisms of heavy metal hyperaccumulation & phytoremediation. J. Trace Elem. Med. Biol., 18(4);339-353.
Yazdani, M., Yap, C.K., Abdullah, F. & Tan, S.G. (2010). An in vitro study on the adsorption, absorption & uptake capacity of Zn by the bioremediator Trichoderma atroviride. Environ. Asia., 3(1);53-59.
Zhang, T., Tang, J., Sun, J., Yu, C., Liu, Z. & Chen, J. (2015), Hex1-related transcriptome of Trichoderma atroviride reveals expression patterns of ABC transporters associated with tolerance to dichlorvos, Biotechnol. Lett., 37(7);1421-1429.
Zin, N.A. & Badaluddin, N.A. (2020). Biological functions of Trichoderma spp. for agriculture applications. Ann. Agric. Sci., 65(2);168-178.