Bioremoval of Pb2+ by Aspergillus niger D1RA, A heavy metal-resistant fungus isolated from an illegal gold mining site

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RISA NOFIANI
RITA MU’IN
HAFIZAH
PUJI ARDININGSIH
https://orcid.org/0000-0003-4311-3016

Abstract

Abstract. Nofiani R, Mu’in R, Hafizah, Ardiningsih P. 2024. Bioremoval of Pb2+ by Aspergillus niger D1RA, A heavy metal-resistant fungus isolated from an illegal gold mining site. Biodiversitas 25: 2504-2511. Heavy metal pollution can cause serious problems for the environment and human health. One of the methods to eliminate this pollution is to use heavy metal-resistant fungi isolated from heavy metal-polluted environments. This study aimed to investigate the ability of heavy metal-resistant fungi to remove Pb2+ in liquid media, Potato Dextrose Broth (PDB). Samples were collected from two locations, namely an abandoned illegal gold mining site and illegal gold mine, Samalantan, Bengkayang District, West Kalimantan, Indonesia. Each sample was inoculated on two different agar media (PDA= Potato Dextrose Agar and MEA= Malt Extract Agar) supplemented with 7.5 ppm HgCl2. All fungal species that grew on the surface media were isolated, identified (based on spore morphology and Internal Transcribed Spacer [ITS]), evaluated (tolerance index [TI] against Hg2+, Pb2+, and Zn2+), and assessed for their bioaccumulation capacity and Pb2+removal efficiency. Four isolates (Aspergillus sp. OK2A, Aspergillus sp. OEA, Aspergillus sp. OEB and OEC) were successfully isolated from the abandoned illegal gold mine, while only one isolate (Aspergillus niger D1RA) was isolated from the illegal gold mining site. On the eighth day of incubation, the high tolerance level of each fungus to various selected metal concentrations was Aspergillus sp. OK2A in 40 ppm HgCl2 and 300 ppm ZnCl2; Aspergillus sp. OEA in 40 ppm HgCl2 and 1,200 ppm ZnCl2; Aspergillus sp. OEB in 800 ppm Pb(NO3)2; OEC in 20 ppm HgCl2; A. niger D1RA in 40 ppm HgCl2, 1,200 ppm Pb(NO3)2, 300 ppm ZnCl2. Only A. niger D1RA showed a high tolerance for three metals and was further analyzed to determine the bioaccumulation capacity and removal efficiency of Pb2+. The best bioaccumulation capacity and removal efficiency of Pb2+ in PDB medium supplemented with 100 ppm Pb(NO3)2 at pH 4 were 237.776 mg/g dried biomass and 93.266 %, respectively. In conclusion, A. niger D1RA has the potential as a bioremediation agent to remediate Pb2+ environments.

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References
Ajsuvakova, O. P., Tinkov, A. A., Aschner, M., Rocha, J. B. T., Michalke, B., Skalnaya, M. G., Skalny, A. V., Butnariu, M., Dadar, M., Sarac, I., Aaseth, J., & Bjørklund, G. (2020). Sulfhydryl groups as targets of mercury toxicity. Coordination Chemistry Reviews, 417, 213343. https://doi.org/10.1016/j.ccr.2020.213343
Bagy, M. M. K., El-Sharouny, H. M. M., & El-Shanawany, A. A. (1991). Effect of pH and organic matter on the toxicity of heavy metals to growth of some fungi. Folia Microbiologica, 36(4), 367–374. https://doi.org/10.1007/BF02814511
Collin, M. S., Venkatraman, S. K., Vijayakumar, N., Kanimozhi, V., Arbaaz, S. M., Stacey, R. G. S., Anusha, J., Choudhary, R., Lvov, V., Tovar, G. I., Senatov, F., Koppala, S., & Swamiappan, S. (2022). Bioaccumulation of lead (Pb) and its effects on human: A review. Journal of Hazardous Materials Advances, 7(May), 0–7. https://doi.org/10.1016/j.hazadv.2022.100094
Doku, T., & Belford, E. (2015). The potential of Aspergillus fumigatus and Aspergillus niger in bioaccumulation of heavy metals from the Chemu Lagoon, Ghana. Journal of Applied Biosciences, 94(1), 8907. https://doi.org/10.4314/jab.v94i1.12
Dursun, A. ., Uslu, G., Cuci, Y., & Aksu, Z. (2003). Bioaccumulation of copper ( II ), lead ( II ) and chromium ( VI ) by growing Aspergillus niger bioaccumulation of copper ( II ), lead ( II ) and chromium ( VI ) by. Process Biochemistry, 38, 1647–1651.
Fazli, M. M., Soleimani, N., Mehrasbi, M., Darabian, S., Mohammadi, J., & Ramazani, A. (2015). Highly cadmium tolerant fungi: Their tolerance and removal potential. Journal of Environmental Health Science and Engineering, 13(1), 1–9. https://doi.org/10.1186/s40201-015-0176-0
Firinc?, C., Zamfir, L. G., Constantin, M., R?ut, I., Capr?, L., Popa, D., Jinga, M. L., Baroi, A. M., Fier?scu, R. C., Corneli, N. O., Postolache, C., Doni, M., Gurban, A. M., Jecu, L., & ?esan, T. E. (2024). Microbial removal of heavy metals from contaminated environments using metal-resistant indigenous strains. Journal of Xenobiotics, 14(1), 51–78. https://doi.org/10.3390/jox14010004
Galgowska, M., & Pietrzak-Fiecko, R. (2021). Cadmium and lead content in selected fungi from Poland and their edible safety assessment. Molecules, 26, 7289.
Hahne, H. C. H., & Kroontje, W. (1973). Significance of pH and chloride Concentration on behavior of heavy metal pollutants: mercury(II), cadmium(II), zinc(II), and lead(II). Journal of Environmental Quality, 2(4), 444–450. https://doi.org/10.2134/jeq1973.00472425000200040007x
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
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
Jing, Y., Li, Z., Li, Y., Lei, G., Li, L., Yang, X., Zhang, Z., & Yang, W. (2021). The Ability of Edible Fungi Residue to Remove Lead in Wastewater. Frontiers in Environmental Science, 9(August), 1–9. https://doi.org/10.3389/fenvs.2021.723087
Larone, H. ., Westblade, F. ., Burd, M. ., Lockhart, R. ., & Procop, W. . (2023). Larone’s Medically Important Fungi: A Guide to Identification. In Andrew’s Disease of the Skin Clinical Dermatology. (7th ed.). Wiley.
Li, C., Zhou, K., Qin, W., Tian, C., Qi, M., Yan, X., & Han, W. (2019). A Review on heavy metals contamination in soil: effects, sources, and remediation techniques. Soil and Sediment Contamination, 28(4), 380–394. https://doi.org/10.1080/15320383.2019.1592108
Liaquat, F., Munis, M. F. H., Haroon, U., Arif, S., Saqib, S., Zaman, W., Khan, A. R., Shi, J., Che, S., & Liu, Q. (2020). Evaluation of metal tolerance of fungal strains isolated from contaminated mining soil of Nanjing, China. Biology, 9(12), 1–12. https://doi.org/10.3390/biology9120469
Navnage, N. P., Mandal, A., Samadhiya, V., Thakur, J. K., Amat, D., Singh, A. B., Manna, M. C., & Patra, A. K. (2020). Tolerance and bioaccumulation of cadmium and lead by endophytic fungi. Journal of the Indian Society of Soil Science, 68(4), 444–449. https://doi.org/10.5958/0974-0228.2020.00035.3
Nofiani, R., Rio, Komalasari, K., Ardiningsih, P., & Santosa, S. J. (2022). Biosorption of Pb2+ using Fusarium sp. RS01, a Hg2+ and Pb2+-resistant indigenous fungus of an abandoned illegal gold mining site. Sains Malaysiana, 51(6), 1753–1764. https://doi.org/10.17576/jsm-2022-5106-12
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
Prakash, S., Prasad, R., & Yadav, P. K. (2023). Assessing the tolerance impact of fungal isolates against lead and zinc heavy metals under controlled conditions. Environment and Ecology, 41(3), 1369–1377. https://doi.org/10.60151/envec/wwsk8473
Priyanka, & Dwivedi, S. K. (2023). Fungi mediated detoxification of heavy metals?: Insights on mechanisms , influencing factors and recent developments. Journal of Water Process Engineering, 53(May), 103800. https://doi.org/10.1016/j.jwpe.2023.103800
Raftos, D., & Radford, J. (2015). Bioaccumulation of heavy metals by fungi. International Journal of Environmental Chemsitry and Chromatography, 1(1), 15–21.
Saikia, B., Ali, M. S., Gogoi, S. H., & Nath, P. D. (2022). Isolation and Characterization of the Mycofloral Diversity in Traditional Assamese Alcoholic Fermentation from India. Asian Journal of Dairy and Food Research, Of. https://doi.org/10.18805/ajdfr.dr-1829
Sanjaya, W. T. A., Khoirunnisa, N. S., Ismiani, S., Hazra, F., & Santosa, D. A. (2021). Isolation and characterization of mercury-resistant microbes from gold mine area in mount pongkor, bogor district, indonesia. Biodiversitas, 22(7), 2656–2666. https://doi.org/10.13057/BIODIV/D220714
Šimonovi?ová, A., Vojtková, H., Nosalj, S., Piecková, E., Švehláková, H., Kraková, L., Drahovská, H., Stalmachová, B., Ku?ová, K., & Pangallo, D. (2021). Aspergillus niger environmental isolates and their specific diversity through metabolite profiling. Frontiers in Microbiology, 12(June), 1–13. https://doi.org/10.3389/fmicb.2021.658010
Širi?, I., Humar, M., Kasap, A., Kos, I., Mio?, B., & Pohleven, F. (2016). Heavy metal bioaccumulation by wild edible saprophytic and ectomycorrhizal mushrooms. Environmental Science and Pollution Research, 23, 18239–18252. https://doi.org/10.1007/s11356-016-7027-0
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
Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7), 3022–3027. https://doi.org/10.1093/molbev/msab120
V?car, C. L., Covaci, E., Chakraborty, S., Li, B., Weindorf, D. C., Fren?iu, T., Pârvu, M., & Podar, D. (2021). Heavy metal?resistant filamentous fungi as potential mercury bioremediators. Journal of Fungi, 7(5). https://doi.org/10.3390/jof7050386
Valix, M., Tang, J. ., & Malik, R. (2001). Heavi metal tolerance of fungi. Minerals Engineering, 14(5), 499–505.
Wang, Y., Yi, B., Sun, X., Yu, L., Wu, L., Liu, W., Wang, D., Li, Y., Jia, R., Yu, H., & Li, X. (2019). Removal and tolerance mechanism of Pb by a filamentous fungus: A case study. Chemosphere, 225, 200–208. https://doi.org/10.1016/j.chemosphere.2019.03.027
Xu, X., Hao, R., Xu, H., & Lu, A. (2020). Removal mechanism of Pb(II) by Penicillium polonicum: immobilization, adsorption, and bioaccumulation. Scientific Reports, 10(1), 1–12. https://doi.org/10.1038/s41598-020-66025-6
Zhang, L., Wang, C., Guo, B., Yuan, Z., & Zhou, X. (2024). Reproductive strategy response of the fungi Sarocladium and the evaluation for remediation under stress of heavy metal Cd(II). Ecotoxicology and Environmental Safety, 271(September 2023), 115967. https://doi.org/10.1016/j.ecoenv.2024.115967