Evaluation of Tolerance and Uptake of Cd and Mn for Microfungi Aspergillus flavus, Aspergillus oryzae, and Aspergillus terreus Isolated from Landfill Soil Collected from Bangar, La Union Philippines 10.32526/ennrj/22/20230254

Main Article Content

Jan Aizel E. Arellano
Irish Benja M. Argame
Francis Ruel G. Castillo
Christian Geen E. Salazar
Mark Kevin S. Lopez

Abstract

Excessive deposition of heavy metals into the environment due to anthropogenic activities necessitates an eco-friendly clean-up strategy. Among microorganisms, limited studies have been made on the mycoremediation potential of microfungi. This paper evaluated three landfill microfungal isolates of Aspergillus species for tolerance and uptake to Cd and Mn. Culture media optimization was also performed for the evaluation of the tolerance index and heavy metal analysis of soil samples from the landfill site. Among the nine heavy metals analyzed, Mn and Fe were detected in relatively high amounts, while Cd, Ni, and Cu were detected in a moderate range. Luxuriant mycelial growth of A. oryzae (MK120548.1) and A. flavus (MH864264.1) was observed in potato dextrose  agar while A. terreus (MH047280.1) grew best in potato sucrose agar. In terms of tolerance index, A. oryzae (MK120548.1) and A. flavus (MH864264.1) demonstrated high tolerance to Cd up to 10 mg/kg. A. oryzae (MK120548.1) showed high tolerance to Mn up to 1,000 mg/kg while A. flavus (MH864264.1) exhibited a very high 10,000 mg/kg tolerance. In terms of metal uptake, A. oryzae (MK120548.1) showed the highest metal uptake of up to 654 mg/kg of Cd,    while A. terreus (MH047280.1) exhibited the highest metal uptake of 997 mg/kg ofMn. With these findings, A. oryzae (MK120548.1), A. flavus (MH864264.1), and A. terreus (MH047280.1) have considerable mycoremediation potential. Bioremediation studies in conjunction with plants can be explored to further assess the potential of these Aspergillus species.

Article Details

How to Cite
Arellano, J. A. E., Argame, I. B. M., Castillo, F. R. G., Salazar, C. G. E., & Lopez, M. K. S. (2024). Evaluation of Tolerance and Uptake of Cd and Mn for Microfungi Aspergillus flavus, Aspergillus oryzae, and Aspergillus terreus Isolated from Landfill Soil Collected from Bangar, La Union Philippines: 10.32526/ennrj/22/20230254. Environment and Natural Resources Journal, 22(2), 184–196. Retrieved from https://ph02.tci-thaijo.org/index.php/ennrj/article/view/250943
Section
Original Research Articles

References

Acosta-Rodríguez I, Cárdenas-González JF, Rodríguez Pérez AS, Oviedo JT, Martínez-Juárez VM. Bioremoval of different heavy metals by the resistant fungal strain Aspergillus niger. Bioinorganic Chemistry Applications 2018;2018:Article No. 3457196.

Aishwarya SA, Nagam N, Vijaya T, Netala RV. Screening and identification of heavy metal-tolerant endophytic fungi Lasiodiplodia theobromae from Boswellia ovalifoliolata an endemic plant of tirumala hills. Asian Journal of Pharmaceutical and Clinical Research 2017;10(3):488-91.

Al-Garni S, Ghanem K, Bahobail A. Biosorption characteristics of Aspergillus fumigatus in removal of cadmium from an aqueous solution. African Journal of Biotechnology 2009;8(17):4163-72.

Al-Obaid AM, Hashem AR. Zinc tolerance and accumulation in Aspergillus oryzae, Penicillium citrinum and Rhizopus stolonifer isolated from Saudi Arabian Soil. Qatar University Science Journal 1997;17(1):103-9.

Alzahrani NH, Alamoudi KH, El-Gendy MM. Molecular identification and nickel biosorption with the dead biomass of some metal tolerant fungi. Journal of Microbial and Biochemical Technology 2017;9(6):310-5.

Ayilara MS, Babalola OO. Bioremediation of environmental wastes: The role of microorganisms. Frontiers in Agronomy 2023;5:Article No. 1183691.

Beinabaj SM, Heydariyan H, Aleii HM, Hosseinzadeh A. Concentration of heavy metals in leachate, soil, and plants in Tehran’s landfill: Investigation of the effect of landfill age on the intensity of pollution. Heliyon 2023;9(1):Article No. 13017.

Chibuike GU, Obiora SC. Heavy metal polluted soils: Effect on plants and bioremediation methods. Applied and Environmental Soil Science 2014;2014:Article No. 752708.

Chiroma TM, Ebewele RO, Hymore FK. Comparative assessment of heavy metal levels in soil, vegetables, and urban grey wastewater used for irrigation in Yola and Kano. International Refereed Journal of Engineering and Science 2014;3(2):1-9.

Doku TE, Belford EJ. The potential of Aspergillus fumigatus and Aspergillus niger in bioaccumulation of heavy metals from the Chemu Lagoon, Ghana. Journal of Applied Biosciences 2015;94:8907-14.

Dulay RM, De Castro ME. Cadmium and chromium tolerance and mycoremediation ability of tiger sawgill mushroom, Lentinus tigrinus. International Journal of Biology, Pharmacy and Allied Sciences 2016;5(11):3003-12.

El-Moselhy KM, Othman AI, Abd El-Azem H, El-Metwally ME. Bioaccumulation of heavy metals in some tissues of fish in the Red Sea, Egypt. Egyptian Journal of Basic and Applied Sciences 2014;1(2):97-105.

Gajewska J, Floryszak-Wieczorek J, Sobieszczuk-Nowicka E, Mattoo A, Arasimowicz-Jelonek M. Fungal and oomycete pathogens and heavy metals: An inglorious couple in the environment. IMA Fungus 2022;13:Article No. 6.

Jamil Emon F, Rohani MF, Sumaiya N, Tuj Jannat MF, Akter Y, Shahjahan M, et al. Bioaccumulation and bioremediation of heavy metals in fishes: A review. Toxics 2023;11(6):1-28.

Joo JH, Hussein KA. Heavy metal tolerance of fungi isolated from contaminated soil. Korean Journal of Soil Science and Fertilizer 2012;45(4):565-71.

Kanmani S, Gandhimathi R. Assessment of heavy metal contamination in soil due to leachate migration from an open dumping site. Applied Water Science 2013;3:193-205.

Khan I, Ali M, Aftab M, Shakir S, Qayyum S, Haleem KS, et al. Mycoremediation: A treatment for heavy metal-polluted soil using indigenous metallotolerant fungi. Environmental Monitoring and Assessment 2019;191:Article No. 622.

Kucher L, Krasnoshtan I, Nedilska U, Muliarchuk O, Manzii O, Menderetsky V, et al. Heavy metals in soil and plants during revegetation of coal mine spoil tips and surrounded territories. Journal of Ecological Engineering 2023;24(7):234-45.

Kumar V, Dwivedi SK. Multimetal tolerant fungus Aspergillus flavus CR500 with remarkable stress response, simultaneous multiple metal/loid removal ability and bioremediation potential of wastewater. Environmental Technology and Innovation 2020;20:Article No. 101075.

Kinuthia GK, Ngure V, Beti D, Lugalia R, Wangila A, Kamau L. Levels of heavy metals in wastewater and soil samples from open drainage channels in Nairobi, Kenya: Community health implication. Scientific Reports 2020;10(1):Article No. 8434.

Li WB, Yao J, Xia FF, Feng HJ, Feng H, Jiang CJ, et al. Leaching behavior of iron from simulated landfills with different operational modes. Bioresource Technology 2011;102(16): 7422-8.

Li X, Li W, Chu L, White Jr. JF, Xiong Z, Li H. Diversity and heavy metal tolerance of endophytic fungi from Dysphania ambrosioides, a hyperaccumulator from Pb-Zn contaminated soils. Journal of Plant Interactions 2016;11(1):186-92.

Liang J, Diao H, Song W, Li L. Tolerance and bioaccumulation of arsenate by Aspergillus oryzae TLWK-09 isolated from arsenic-contaminated soils. Water, Air and Soil Pollution 2018;229:Article No. 169.

Liaquat F, Munis MF, Haroon U, Arif S, Saqib S, Zaman W, et al. Evaluation of metal tolerance of fungal strains isolated from contaminated mining soil of Nanjing, China. Biology 2020;9(12):Article No. 469.

Long DD, Fu RR, Han JR. Tolerance and stress response of sclerotiogenic Aspergillus oryzae G15 to copper and lead. Folia Microbiologica 2017;62:295-304.

Lopez MK. Characterization, molecular identification, and phylogenetic analysis of microfungi isolated from the Landfill Site of Bangar, La Union, Philippines. International Journal of Agricultural Technology 2023;19(3):1085-96.

Lopez MKS, Kalaw SP, Dulay RMR, De Leon AM, Reyes RG. Optimization of mycelial growth of Xylaria papulis Lloyd (Xylariaceae) in indigenous liquid culture conditions, Science City of Muñoz, Nueva Ecija, Philippines. Studies in Fungi 2022;7(21):1-7.

Mahmoud A, Massoud M, Abdel-Motaal F, El-Zayat S. Tolerance and biosorption of manganese, iron and aluminium by five Aspergillus species isolated from freshwater. The International Journal of Environmental Sciences 2017;16(1):61-9.

Nyiramigisha P, Komariah, Sajidan. Harmful impacts of heavy metal contamination in the soil and crops grown around dumpsites. Reviews in Agricultural Science 2021;9:271-82.

Ojekunle OZ, Ojekunle OV, Adeyemi AA, Taiwo AG, Sangowusi OR, Taiwo AM, et al. Evaluation of surface water quality indices and ecological risk assessment for heavy metals in scrap yard neighbourhood. SpringerPlus 2016;5(1):Article No. 560.

Oladipo OG, Awotoye OO, Olayinka A, Bezuidenhout CC, Maboeta MS. Heavy metal tolerance traits of filamentous fungi isolated from gold and gemstone mining sites. Brazilian Journal of Microbiology 2018;49(1):29-37.

Oladipo OG, Awotoye OO, Olayinka A, Ezeokoli OT, Maboeta MS, Bezuidenhout CC. Heavy metal tolerance potential of Aspergillus strains isolated from mining sites. Bioremediation Journal 2016;20(4):287-97.

Oso BA, Olagunji MO, Okiki PA. Lead tolerance and bioadsorption potentials of indigenous soil fungi in Ado Ekiti, Nigeria. European Journal of Experimental Biology 2015; 5(9):15-9.

Palanivel TM, Pracejus B, Novo LAB. Bioremediation of copper using indigenous fungi Aspergillus species isolated from an abandoned copper mine soil. Chemosphere 2023;314:Article No. 137688.

Pawlowska TE, Charvat I. Heavy-metal stress and developmental patterns of arbuscular mycorrhizal fungi. Applied and Environmental Microbiology 2004;70(11):6643-9.

Priyadarshini E, Priyadarshini SS, Cousins BG, Pradhan N. Metal-Fungus interaction: Review on cellular processes underlyingheavy metal detoxification and synthesis of metal nanoparticles. Chemosphere 2021;274:Article No. 129976.

Rashid A, Schutte BJ, Ulery A, Deyholos MK, Sanogo S, Lehnhoff EA, et al. Heavy metal contamination in agricultural soil: Environmental pollutants affecting crop health. Agronomy 2023;13(6):Article No.1521.

Rice EW, Baird RB, Eaton AD. Standard Methods for the Examination of Water and Wastewater. 23rd ed. USA. American Public Health Association; 2017.

Saba G, Thirumarimurugan M, Sivakumar VM. Heavy metal tolerance potential of fungus isolated from copper smelting industry. International Research Journal of Pharmacy 2017;8(6):120-5.

Saha BC, Kennedy GJ. Phosphate limitation alleviates the inhibitory effect of manganese on itaconic acid production by Aspergillus terreus. Biocatalysis and Agricultural Biotechnology 2019;18:Article No. 101016.

Sándor E, Kolláth IS, Fekete E, Bíró V, Flipphi M, Kovács B, et al. Carbon-source dependent interplay of copper and manganese ions modulates the morphology and itaconic acid production in Aspergillus terreus. Frontiers in Microbiology 2021;12:Article No. 680420.

Shakya M, Sharma P, Meryem SS, Mahmood Q, Kumar A. Heavy metal removal from industrial wastewater using fungi: Uptake mechanism and biochemical aspects. Journal of Environmental Engineering 2016;142(9):1-18.

Singh J, Kalamdhad AS. Effects of heavy metals on soil, plants, human health and aquatic life. International Journal of Research in Chemistry and Environment 2011;1(2):15-21.

Singh D, Rathod V, Ninganagouda S, Hiremath J, Singh AK, Mathew J. Optimization and characterization of silver nanoparticle by endophytic fungi Penicillium sp. isolated from Curcuma longa (turmeric) and application studies against MDR E. coli and S. aureus. Bioinorganic Chemistry and Applications 2014;2014:Article No. 408021.

Soleimani N, MohammadianFazli M, Ramazani A, Mehrasbi MR. Application of live, dead and dried biomasses of Aspergillus versicolor for cadmium biotreatment. Journal of Human, Environment and Health Promotion 2016;1(2):87-98.

Sule AM, Inuwa B, Bello SZ, Gero M, Mohammed HA, Muhammad ZA. Isolation, characterization and heavy metals tolerance indices of indigenous fungal flora from a tannery located at Challawa Industrial Estate of Kano State, Nigeria. Journal of Applied Sciences and Environmental Management 2022;26(7):1289-98.

Thabit TMA, El-Naggar MAH. Potential impact of some soil-borne fungi on biodegradation of some organophosphorous-nematicides. American Journal of Environmental Protection 2014;3(6):299-304.

Tiwari S, Lata C. Heavy metal stress, signaling, and tolerance due to plant-associated microbes: An overview. Frontiers in Plant Science 2018;9:Article No. 452.

Upadhyaya H, Panda SK, Bhattacharjee MK, Dutta S. Role of arbuscular mycorrhiza in heavy metal tolerance in plants: Prospects for phytoremidiation. Journal of Phytological Research 2010;2(7):16-27.

Vajpai S, Taylor PE, Adholeya A, Ackland ML. Chromium tolerance and accumulation in Aspergillus flavus isolated from tannery effluent. Journal of Basic Microbiology 2019; 60(1):58-71.

Verma S, Kuila A. Bioremediation of heavy metals by microbial process. Environmental Technology and Innovation 2019;14: Article No. 100369.

Villalba-Villalba AG, González-Méndez B. Evaluating Aspergillus terreus tolerance to toxic metals. Revista Chapingo Serie Ciencias Forestales y del Ambiente 2021;27(3):449-64.

Wang Y, Pleasant S, Dubey B, Rhue D, Bonzongo JC, Townsend T. Assessing the propensity of landfill soils to undergo reductive iron dissolution. Environmental Earth Science 2018;77(8):Article No. 306.

World Health Organization (WHO). Permissible Limits of Heavy Metals in Soil and Plants. Geneva, Switzerland: World Health Organization; 1996.

Wijaya N, Priyani N, Munir E. Lead accumulation activity of fungi isolated from Batang Toru, South Tapanuli, North Sumatra. Proceedings of the IOP Conference Series: Earth and Environmental Science; 2018 Dec 8-9; Medan, North Sumatera, Indonesia; 2019.

Zango UU, Muhammad II, Sharma V, Sharma AK. Effective bioremediation of Cd, Cr, and Pb in tannery effluent using Aspergillus fumigatus and Aspergillus terreus: Synergistic effects of using the two strainst. Water Air and Soil Pollution 2023;234(12):Article No. 735.