Lead (II) Tolerance and Uptake Capacities of Fungi Isolated from a Polluted Tributary in the Philippines

VIEWS - 61 (Abstract) 24 (PDF)
Zomesh Artus Nath Maini, Kiara Marie J. Aribal, Regine Marinelli A. Narag, Jeorgina Kamella Luanshya T. Melad, Juan Angelo D. Frejas, Luis Alfonso M. Arriola, Pia Clarisse Ramos Gulpeo, Ian A. Navarrete, Crisanto M. Lopez


The Lead [Pb(II)] tolerance and uptake ability of four fungal species, two from the genus Penicillium and two from the genus Talaromyces were investigated in this study. The species were isolated from a polluted tributary and identified to be closest to P. canescens, P. simplicissimum, T. macrosporus and another Talaromyces sp. via PCR targeting their internal transcribed spacer 1 and 4 sequences. All isolates have tolerances for up to 2000 µg/mL and 3000 µg/mL Pb(II) on solid and liquid medium, respectively. Both Penicillium isolates have increasing removal rates dependent on initial Pb(II) concentration at 500 to 2000 µg/mL, while removal rates of both Talaromyces isolates are not significantly influenced by initial Pb(II) concentrations. The Pb(II) uptake of all isolates increases with increasing Pb(II) concentration but is depressed at 3000 µg/mL, with the exception of T. macrosporus. The recorded total uptake capacities for both Penicillium isolates in this study are higher than in most literature, at 7.0 – 407.4 mg/g and 50.8 – 412.6 mg/g for P. canescens and P. simplicissimum, respectively. The study also reports the exemplary Pb(II) uptake capacities of both Talaromyces isolates at 58.9 – 601.0 mg/g and 60.9 – 402.3 mg/g for T. macrosporus and Talaromyces sp., respectively.


Mycoremediation; Tolerance Index; Biosorption; Bioaccumulation; Heavy Metals

Full Text:



Say, R., Yilmaz, N., & Denizli, A. (2003). Biosorption of cadmium, lead, mercury, and arsenic ions by the fungus Penicillium purpurogenum. Separation Science and Technology, 38(9), 2039–2053. https://doi.org/10.1081/SS-120020133

He, J., & Chen, J. P. (2014). A comprehensive review on biosorption of heavy metals by algal biomass: Materials, performances, chemistry, and modeling simulation tools. Bioresource Technology, 160, 67–78. https://doi.org/10.1016/j.biortech.2014.01.068

Chen, S. H., Ng, S. L., Cheow, Y. L., & Ting, A. S. Y. (2017). A novel study based on adaptive metal tolerance behavior in fungi and SEM-EDX analysis. Journal of Hazardous Materials, 334, 132–141. https://doi.org/10.1016/j.jhazmat.2017.04.004

Elia, A. C., Galarini, R., Dörr, A. J. M., & Taticchi, M. I. (2006). Bioaccumulation of heavy metals, organochlorine pesticides, and detoxication biochemical indexes in tissues of Ictalurus melas of Lake Trasimeno. Bulletin of Environmental Contamination and Toxicology, 76(1), 132–139. https://doi.org/10.1007/s00128-005-0899-1

Wong, D. L., Merrifield-macrae, M. E., & Stillman, M. J. (2017). Lead (II) Binding in Metallothioneins, 17(Ii), 241–269. https://doi.org/10.1515/9783110434330-009

He, Z. L., Yang, X. E., & Stoffella, P. J. (2005). Trace elements in agroecosystems and impacts on the environment. Journal of Trace Elements in Medicine and Biology, 19(2–3), 125–140. https://doi.org/10.1016/j.jtemb.2005.02.010

Singh, R., Gautam, N., Mishra, A., & Gupta, R. (2011). Heavy metals and living systems: An overview. Indian Journal of Pharmacology, 43(3), 246. https://doi.org/10.4103/0253-7613.81505

Tong, S., Schirnding, Y. E. V., & Prapamontol, T. (2000). Environmental lead exposure: a public health problem of global dimensions. Bulletin of the World Health Organization, 78, 1068-1077.

Kim, H. C., Jang, T. W., Chae, H. J., Choi, W. J., Ha, M. N., Ye, B. J., ... & Hong, Y. S. (2015). Evaluation and management of lead exposure. Annals of occupational and environmental medicine, 27(1), 30. https://doi.org/10.1186/s40557-015-0085-9

Ona, L. F., Alberto, A. M. P., Prudente, J. A., & Sigua, G. C. (2006). Levels of lead in urban soils from selected cities in a central region of the Philippines. Environmental Science and Pollution Research, 13(3), 177–183. https://doi.org/10.1065/espr2005.08.275

Riddell, T. (2007). Elevated blood-lead levels among children living in the rural Philippines. Bulletin of the World Health Organization, 85(9), 674–680. https://doi.org/10.2471/blt.06.036137

Solon, O., Riddell, T., Quimbo, S., Butrick, E., Alyward, G., Bacate, M., & Peabody, J. (2008). Nutrition among Children in the Central Philippines. Journal of Pediatrics, 152(2), 237–244. https://doi.org/10.1016/j.jpeds.2007.09.008

Navarrete, I. A., Gabiana, C. C., Dumo, J. R. E., Salmo, S. G., Guzman, M. A. L. G., Valera, N. S., & Espiritu, E. Q. (2017). Heavy metal concentrations in soils and vegetation in urban areas of Quezon City, Philippines. Environmental monitoring and assessment, 189(4), 145. https://doi.org/10.1007/s10661-017-5849-y

Ayangbenro, A. S., & Babalola, O. O. (2017). A new strategy for heavy metal polluted environments: A review of microbial biosorbents. International Journal of Environmental Research and Public Health, 14(1), 1 – 16. https://doi.org/10.3390/ijerph14010094

Dixit, R., Malaviya, D., Pandiyan, K., Singh, U. B., Sahu, A., Shukla, R., … Paul, D. (2015). Bioremediation of Heavy Metals from Soil and Aquatic Environment: An Overview of Principles and Criteria of Fundamental Processes. Sustainability, 7(2), 2189–2212. https://doi.org/10.3390/su7022189

Kapahi, M., & Sachdeva, S. (2017). Mycoremediation potential of Pleurotus species for heavy metals: a review. Bioresources and Bioprocessing, 4(1), 1 – 9 https://doi.org/10.1186/s40643-017-0162-8

Oladipo, O. G., Awotoye, O. O., Olayinka, A., Bezuidenhout, C. C., & Maboeta, M. S. (2018). Heavy metal tolerance traits of filamentous fungi isolated from gold and gemstone mining sites. Brazilian Journal of Microbiology, 49(1), 29–37. https://doi.org/10.1016/j.bjm.2017.06.003

Kalac, P., & Svoboda, L. (2000). A review of trace element concentrations in edible mushrooms. Food Chemistry, 69, 273–281. https://doi.org/10.1016/S0308-8146(99)00264-2

Gube M. (2016) Fungal Molecular Response to Heavy Metal Stress. In: Esser, K., Hoffmeister, D. (eds) Biochemistry and Molecular Biology. The Mycota (A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research) vol III (pp. 47-68), Cham, Switzerland: Springer. https://doi.org/10.1007/978-3-319-27790-5_4

Rhodes, C. J. (2014). Mycoremediation (bioremediation with fungi) - growing mushrooms to clean the earth. Chemical Speciation and Bioavailability, 26(3), 196–198. https://doi.org/10.3184/095422914X14047407349335

Gadd, G. M. (2007). Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycological Research, 111(1), 3–49. https://doi.org/10.1016/j.mycres.2006.12.001

Bellion, M., Courbot, M., Jacob, C., Blaudez, D., & Chalot, M. (2006). Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiology Letters, 254(2), 173–181. https://doi.org/10.1111/j.1574-6968.2005.00044.x

Iskandar, N. L., Zainudin, N. A. I. M., & Tan, S. G. (2011). Tolerance and biosorption of copper (Cu) and lead (Pb) by filamentous fungi isolated from a freshwater ecosystem. Journal of Environmental Sciences, 23(5), 824–830. https://doi.org/10.1016/S1001-0742(10)60475-5

Joshi, P. K., Swarup, A., Maheshwari, S., Kumar, R., & Singh, N. (2011). Bioremediation of Heavy Metals in Liquid Media Through Fungi Isolated from Contaminated Sources. Indian Journal of Microbiology, 51(4), 482–487. https://doi.org/10.1007/s12088-011-0110-9

Romero, M. C., Reinoso, E. H., Urrutia, M. I., & Kiernan, A. M. (2006). Biosorption of heavy metals by Talaromyces helicus: A trained fungus for copper and biphenyl detoxification. Electronic Journal of Biotechnology, 9(3), 221–226. https://doi.org/10.1016/j.toxlet.2006.04.004

Abd El Hameed, A. H., Eweda, W. E., Abou-Taleb, K. A. A., & Mira, H. I. (2015). Biosorption of uranium and heavy metals using some local fungi isolated from phosphatic fertilizers. Annals of Agricultural Sciences, 60(2), 345–351. https://doi.org/10.1016/j.aoas.2015.10.003

Machido, D., Ezeonuegbu, B., & Yakubu, S. E. (2011). Capacity of Isolates of Six Genera of Filamentous Fungi to Remove Lead, Nickel and Cadmium from Refinery Effluent. Journal of Environment and Earth Science, 6(8), 72–76. Retrieved from http://iiste.org/Journals/index.php/JEES/article/view/32545

Zhang, S., Zhang, X., Chang, C., Yuan, Z., Wang, T., Zhao, Y., … Li, X. (2016). Improvement of tolerance to lead by filamentous fungus Pleurotus ostreatus HAU-2 and its oxidative responses. Chemosphere, 150, 33–39. https://doi.org/10.1016/j.chemosphere.2016.02.003

Ostrea, E. M., Ostrea, A. M., Villanueva-Uy, M. E., Chiodo, L., & Janisse, J. (2015). Alluvial and riparian soils as major sources of lead exposure in young children in the Philippines: the role of floods. Environmental Science and Pollution Research, 22(7), 5082–5091. https://doi.org/10.1007/s11356-014-3908-2

Ellis, M. B., & Ellis J.P. (1997). Microfungi on Land Plants: An Identification Handbook, (pp. 1 – 868), Croom Helm, London: Richmond Publishers.

Gilman, J. C. (2001). A Manual of Soil Fungi, 2nd ed., (pp. 1 – 400), New Delhi, India: Daya Publishing.

Nagamani, A., Kunwar, I. K., Manoharachary, C. (2006). Handbook of Soil Fungi, (pp 1 – 477), New Delhi, India: K. International Pvt. Ltd.

Dey, P., Gola, D., Mishra, A., Malik, A., Singh, D. K., Patel, N., … Jehmlich, N. (2016). Comparative performance evaluation of multi-metal resistant fungal strains for simultaneous removal of multiple hazardous metals. Journal of Hazardous Materials, 318, 679–685. https://doi.org/10.1016/j.jhazmat.2016.07.025

Mohsenzadeh, F., & Shahrokhi, F. (2014). Biological removing of Cadmium from contaminated media by fungal biomass of Trichoderma species. Journal of Environmental Health Science and Engineering, 12(1), 1–7. https://doi.org/10.1186/2052-336X-12-102

Kiene, R. P., & Slezak, D. (2006). Low dissolved DMSP concentrations in seawater revealed by small-volume gravity filtration and dialysis sampling. Limnology and Oceanography: Methods, 4(4), 80–95. https://doi.org/10.4319/lom.2006.4.80

Zucconi, L., Ripa, C., Alianiello, F., Benedetti, A., & Onofri, S. (2003). Lead resistance sorption accumulation in a Paecilomyces lilacinus strain. Biology and Fertility of Soils, 37(1), 17–22. https://doi.org/10.1007/s00374-002-0555-4

Zafar, S., Aqil, F., & Ahmad, I. (2007). Metal tolerance and biosorption potential of filamentous fungi isolated from metal contaminated agricultural soil. Bioresource Technology, 98(13), 2557–2561. https://doi.org/10.1016/j.biortech.2006.09.051

Valix, M., & Loon, L. O. (2003). Adaptive tolerance behaviour of fungi in heavy metals. Minerals Engineering, 16(3), 193–198. https://doi.org/10.1016/S0892-6875(03)00004-9

Valix, M., Tang, J. Y., & Malik, R. (2001). Heavy metal tolerance of fungi. Minerals Engineering, 14(5), 499–505. https://doi.org/10.1016/s0892-6875(01)00037-1

Gorbushina A.A., Krumbein W.E. (2000). Subaerial Microbial Mats and Their Effects on Soil and Rock. In: Riding R.E., Awramik S.M. (eds) Microbial Sediments, (pp 161–170), Berlin, Germany: Springer. https://doi.org/10.1007/978-3-662-04036-2_18

Iram, S., Ahmad, I., Javed, B., Yaqoob, S., Akhtar, K., Kazmi, M. R., & Badar-uz-Zaman. (2009). Fungal tolerance to heavy metals. Pakistan Journal of Botany, 41(5), 2583–2594.

Leitão, A. L. (2009). Potential of Penicillium species in the bioremediation field. International Journal of Environmental Research and Public Health, 6(4), 1393–1417. https://doi.org/10.3390/ijerph6041393

Ezzouhri, L., Castro, E., Moya, M., Espinola, F., & Lairini, K. (2009). Heavy metal tolerance of filamentous fungi isolated from polluted sites in Tangier, Morocco. African Journal of Microbiology Research, 3(2), 35–48. https://doi.org/10.4236/nr.2012.34022

Jacob, J.M., Bardhan, S., & Balakrishnan R.B. (2013). Selenium and Lead tolerance in fungi isolated from sea water. International Journal of Innovative Research in Science, Engineering and Technology, 2(7), 2975 – 2982.

Chojnacka, K. (2010). Biosorption and bioaccumulation - the prospects for practical applications. Environment International, 36(3), 299–307. https://doi.org/10.1016/j.envint.2009.12.001

Hafez, N., AbdelRazek, A. S., & Hafez, M. B. (1997). Accumulation of some heavy metals on Aspergillus flavus. Journal of Chemical Technology and Biotechnology, 68(1), 19–22. https://doi.org/10.1002/(sici)1097-4660(199701)68:1<19::aid-jctb508>3.0.co;2-k

Oso, B. A., Olagunji, M.O., & Okiki, P.A. (2015). Lead tolerance and bioadsorption potentials of indigenous soil fungi in Ado Ekiti, Nigeria. European Journal of Experimental Biology, 5(9), 15 – 19.

Aytar, P., Gedikli, S., Buruk, Y., Cabuk, A., & Burnak, N. (2014). Lead and nickel biosorption with a fungal biomass isolated from metal mine drainage: Box-Behnken experimental design. International Journal of Environmental Science and Technology, 11(6), 1631–1640. https://doi.org/10.1007/s13762-013-0354-5

Svecova, L., Spanelova, M., Kubal, M., & Guibal, E. (2006). Cadmium, lead and mercury biosorption on waste fungal biomass issued from fermentation industry. I. Equilibrium studies. Separation and Purification Technology, 52(1), 142–153. https://doi.org/10.1016/j.seppur.2006.03.024

Fan, T., Liu, Y., Feng, B., Zeng, G., Yang, C., Zhou, M., … Wang, X. (2008). Biosorption of cadmium(II), zinc(II) and lead(II) by Penicillium simplicissimum: Isotherms, kinetics and thermodynamics. Journal of Hazardous Materials, 160(2–3), 655–661. https://doi.org/10.1016/j.jhazmat.2008.03.038

Say, R., Yilmaz, N., & Denizli, A. (2003b). Removal of Heavy Metal Ions Using the Fungus Penicillium canescens. Adsorption Science & Technology, 21(7), 643–650. https://doi.org/10.1260/026361703772776420

Šimonovičová, A. (2008). Use of mitosporic fungi for heavy metal removal from experimental water solutions. Czasopismo Techniczne, 105(2): 207-212.

Massaccesi, G., Romero, M. C., Cazau, M. C., & Bucsinszky, A. M. (2002). Cadmium removal capacities of filamentous soil fungi isolated from industrially polluted sediments, in La Plata (Argentina). World Journal of Microbiology and Biotechnology, 18(9), 817–820. https://doi.org/10.1023/A:1021282718440

Wang, N., Xu, X., Li, H., Wang, Q., Yuan, L., & Yu, H. (2017). High performance and prospective application of xanthate-modified thiourea chitosan sponge-combined Pseudomonas putida and Talaromyces amestolkiae biomass for Pb(II) removal from wastewater. Bioresource Technology, 233, 58–66. https://doi.org/10.1016/j.biortech.2017.02.069

Bengtsson, L., Johansson, B., Hackett, T. J., McHale, L., & McHale, A. P. (1995). Studies on the biosorption of uranium by Talaromyces emersonii CBS 814.70 biomass. Applied Microbiology and Biotechnology, 42(5), 807–811. https://doi.org/10.1007/BF00171965

Yetis, U., Dolek, A., Dilek, F. B., & Ozcengiz, G. (2000). The removal of Pb(II) by Phanerochaete chrysosporium. Water Research, 34(16), 4090–4100. https://doi.org/10.1016/S0043-1354(00)00155-X

Jentschke, G., & Godbold, D. L. (2000). Metal toxicity and ectomycorrhizas. Physiologia Plantarum, 109(2), 107–116. https://doi.org/10.1034/j.1399-3054.2000.100201.x

Melgar, M. J., Alonso, J., & García, M. A. (2007). Removal of toxic metals from aqueous solutions by fungal biomass of Agaricus macrosporus. Science of the Total Environment, 385(1–3), 12–19. https://doi.org/10.1016/j.scitotenv.2007.07.011

Adeogun, A. I., Kareem, S. O., Durosanya, J. B., & Balogun, E. S. (2012). Kinetics and Equilibrium Parameters of Biosorption and Bioaccumulation of Lead Ions From Aqueous Solutions By. Journal of Microbiology, Biotechnology and Food Sciences, 1(5), 1221–1234.

Akar, T., & Tunali, S. (2006). Biosorption characteristics of Aspergillus flavus biomass for removal of Pb(II) and Cu(II) ions from an aqueous solution. Bioresource Technology, 97(15), 1780–1787. https://doi.org/10.1016/j.biortech.2005.09.009

Ahmad, I., Ahmad, F., & Pichtel, J. (2011). Metal Tolerance and Biosorption Potential of Soil Fungi: Applications for a Green and Clean Water Treatment Technology. In: Ahmad, I., Ahmad, F., & Pitchel, J. (eds) Microbes and microbial technology: Agricultural and environmental applications (pp 321 – 361), New York, USA: Springer-Verlag. https://doi.org/10.1007/978-1-4419-7931-5_13

Bulut, Y., & Baysal, Z. (2006). Removal of Pb(II) from wastewater using wheat bran. Journal of Environmental Management, 78(2), 107–113. https://doi.org/10.1016/j.jenvman.2005.03.010

Sun, F., & Shao, Z. (2007). Biosorption and bioaccumulation of lead by Penicillium sp. Psf-2 isolated from the deep sea sediment of the Pacific Ocean. Extremophiles, 11(6), 853–858. https://doi.org/10.1007/s00792-007-0097-7

Acharya, C., Acharya, S., Kar, R.N., & Sukla, L.B. (1999) Toxic Effect of Lead on the growth of Penicillium species. Journal of the Indian Institute of Science, 79, 295 – 302.

Iram, S., Shabbir, R., Zafar, H., & Javaid, M. (2015). Biosorption and Bioaccumulation of Copper and Lead by Heavy Metal-Resistant Fungal Isolates. Arabian Journal for Science and Engineering, 40(7), 1867–1873. https://doi.org/10.1007/s13369-015-1702-1

Yalçin, E., Çavuşoĝlu, K., & Kinalioĝlu, K. (2010). Biosorption of Cu2+and Zn2+by raw and autoclaved Rocella phycopsis. Journal of Environmental Sciences, 22(3), 367–373. https://doi.org/10.1016/S1001-0742(09)60117-0

Aksu, Z., & Tezer, S. (2005). Biosorption of reactive dyes on the green alga Chlorella vulgaris. Process Biochemistry, 40(3–4), 1347–1361. https://doi.org/10.1016/j.procbio.2004.06.007

Taboski, M. A. S., Rand, T. G., & Piórko, A. (2005). Lead and cadmium uptake in the marine fungi Corollospora lacera and Monodictys pelagica. FEMS Microbiology Ecology, 53(3), 445–453. https://doi.org/10.1016/j.femsec.2005.02.009

Vodnik, D., Byrne, A. R., & Gogala, N. (1998). The uptake and transport of lead in some ectomycorrhizal fungi in culture. Mycological Research, 102(8), 953–958. https://doi.org/10.1017/S0953756297005959

Udochukwu, U., Nekpen, B. O., Udinyiwe, O. C., & Omeje, F. I. (2014). Bioaccumulation of heavy metals and pollutants by edible mushroom collected from Iselu market Benin-city. International Journal of Current Microbiology and Applied Sciences, 3(10), 52–57.


  • There are currently no refbacks.

Copyright (c) 2019 Zomesh Artus Nath Maini, Zomesh Artus Nath Maini, Kiara Marie J. Aribal, Regine Marinelli A. Narag, Jeorgina Kamella Luanshya T. Melad, Juan Angelo D. Frejas, Luis Alfonso M. Arriola, Pia Clarisse Ramos Gulpeo, Ian A. Navarrete, Crisanto M. Lopez

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.