Potencial de la biomasa fúngica: producción y mecanismos de biorremediación de metales pesados del compost de residuos sólidos orgánicos municipales

W. E.  Nuñez; D. A.  Sotomayor; C. V.  Ballardo; E.  Herrera

doi:10.17268/sci.agropecu.2023.008

Authors

W. E. Nuñez Centro de Investigación en Gestión de Residuos Sólidos, Universidad Nacional del Centro del Perú, Av. Mariscal Castilla N° 3909, Junín.
D. A. Sotomayor Doctorado en Ingeniería y Ciencias Ambientales, Universidad Nacional Agraria La Molina, Av. La Molina s/n, 15464, Lima.
C. V. Ballardo Centro de Investigación en Gestión de Residuos Sólidos, Universidad Nacional del Centro del Perú, Av. Mariscal Castilla N° 3909, Junín.
E. Herrera Instituto de Investigación Especializado de Investigación de la Facultad de Zootecnia, Universidad Nacional del Centro del Perú, Av. Mariscal Castilla N° 3909, Junín.

DOI:

https://doi.org/10.17268/sci.agropecu.2023.008

Keywords:

Fungal biomass, compostaje, bioremediation, metals, organic waste

Abstract

The compost produced based on municipal/urban organic solid waste (RSOM/U), is a valuable resource as a biofertilizer for agriculture, gardening, forestry and especially for soil remediation, whose production contributes to sustainable development through recycling of organic matter and nutrients. However, due to the raw materials used, the compost can have a significant content of heavy metals such as: cadmium (Cd), lead (Pb), arsenic (As), mercury (Hg) and selenium (Se), and contaminants such as potentially toxic trace elements that harm human health. These components can accumulate in plant tissues by absorption, giving rise to the possibility of being bioavailable to humans and animals. The fungal bioremediation of heavy metals in RSOM/U compost is highly efficient, cost-effective, available and friendly to the environment, therefore the removal of metals through this technique is a priority, if the purpose is to use it in agricultural soils. This review summarizes the studies based on the potential of fungal biomass for the bioremediation of heavy metals in RSOM/U compost, reporting information on RSOM/U-based compost, fungal biomass production and mechanisms of bioremediation of heavy metals by fungal biomass. In conclusion, the bioremediation of heavy metals using the fungal biomass in RSOM/U compost, with adequate segregation of raw material, coupled with bioremediation, could improve the removal of heavy metals in RSOM/U compost, and could be an ecological and viable alternative, which must be valued by intensifying its use.

References

Abraham, S., García, J., & Peña, J. J. (2015). Microorganisms role in the bioremediation of contaminated soils with heavy metals. Acta Universitaria, 25(NE-3), 40-45.

Ahmed, S., Mustafa, G., Arshad, M., & Rajoka, M. I. (2017). Fungal Biomass Protein Production from Trichoderma harzianum Using Rice Polishing. BioMed Research International, 2017.

Arévalo, E., Cayotopa, J., Olivera, D., Gárate, M., Trigoso, E., Costa, B., & Leon, B. (2017). Optimización de sustratos para la producción de conidias de Trichoderma harzianum. Por fermentación sólida en la región de San Martín. Perú. Rev. investig. Altoandin, 19(2), 135-144.

Atagana, H. I. (2009). Biodegradation of PAHs by fungi in contaminated-soil containing cadmium and nickel ions. African Journal of Biotechnology, 8(21), 5780-5789.

Australiana, N. (2001). Ordenanza del Ministro Federal de Agricultura, Silvicultura, Medio Ambiente y Gestión del Agua sobre los requisitos de calidad para compost a partir de desechos (Ordenaza sobre Compost). Bundesgesetzblatt Für Die Republik Österreich, 1723-1745.

Awasthi, S. K., Duan, Y., Liu, T., Zhang, Z., Pandey, A., et al. (2021). Can biochar regulate the fate of heavy metals (Cu and Zn) resistant bacteria community during the poultry manure composting? Journal of Hazardous Materials, 406, 124593.

Awasthi, S. K., Sarsaiya, S., Awasthi, M. K., Liu, T., Zhao, J., Kumar, S., & Zhang, Z. (2020). Changes in global trends in food waste composting: Research challenges and opportunities. Bioresource Technology, 299(September 2019), 122555.

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).

Babu, A. G., Shim, J., Bang, K. S., Shea, P. J., & Oh, B. T. (2014). Trichoderma virens PDR-28: A heavy metal-tolerant and plant growth-promoting fungus for remediation and bioenergy crop production on mine tailing soil. Journal of Environmental Management, 132, 129-134.

Baldrian, P., In Der Wiesche, C., Gabriel, J., Nerud, F., & Zadražil, F. (2000). Influence of cadmium and mercury on activities of ligninolytic enzymes and degradation of polycyclic aromatic hydrocarbons by Pleurotus ostreatus in soil. Applied and Environmental Microbiology, 66(6), 2471-2478.

Barthod, J., Rumpel, C., & Dignac, M. F. (2018). Composting with additives to improve organic amendments. A review. Agronomy for Sustainable Development, 38(2).

Beltrán-Pineda, M. E., & Gómez-Rodríguez, A. M. (2016). Biorremediación de metales pesados cadmio (Cd), cromo (Cr) y mercurio (Hg), mecanismos bioquímicos e ingeniería genética: una revisión. Revista Facultad de Ciencias Básicas, 12(2), 172-197.

Cadavid-Velásquez, E. D. J., Pérez-Vásquez, N. D. S., & Marrugo-Negrete, J. (2019). Contaminación por metales pesados en la bahía Cispatá en Córdoba-Colombia y su bioacumulación en macromicetos. Gestión y Ambiente, 22(1), 43-53.

Campuzano, R., & González-Martínez, S. (2016). Characteristics of the organic fraction of municipal solid waste and methane production: A review. Waste Management, 54, 3-12.

Cao, Y., Wang, X., Zhang, X., Misselbrook, T., Bai, Z., & Ma, L. (2021). An electric field immobilizes heavy metals through promoting combination with humic substances during composting. Bioresource Technology, 330(February).

Cao, Y., Zhao, J., Wang, Q., Bai, S., Yang, Q., Wei, Y., & Wang, R. (2022). Industrial aerobic composting and the addition of microbial agents largely reduce the risks of heavy metal and ARG transfer through livestock manure. Ecotoxicology and Environmental Safety, 239(May), 113694.

Carhuavilca, D., Sànhez, A., Robles, J. L., Vásquez, J., Blas, R., Quispe, E., & Huauya, A. (2021). Perú: Anuario de Estadísticas Ambientales 2021. Instituto Nacional de Estadística e Informática. 540.

Cerda, A., Artola, A., Barrena, R., Font, X., Gea, T., & Sánchez, A. (2019). Innovative Production of Bioproducts From Organic Waste Through Solid-State Fermentation. Frontiers in Sustainable Food Systems, 3.

Chen, H., Dou, J., & Xu, H. (2018). Remediation of Cr(VI)-contaminated soil with co-composting of three different biomass solid wastes. Journal of Soils and Sediments, 18(3), 897-905.

Chen, X., Zhao, Y., Zhang, C., Zhang, D., Yao, C., et al. (2020). Speciation, toxicity mechanism and remediation ways of heavy metals during composting: A novel theoretical microbial remediation method is proposed. Journal of Environmental Management, 272(June 2019), 111109.

Covarrubias, S. A., García Berumen, J. A., & Peña Cabriales, J. J. (2015). Microorganisms role in the bioremediation of contaminated soils with heavy metals. Acta Universitaria, 25(NE-3), 40-45.

Cubillos, M., Wulff, J. N., & Wøhlk, S. (2021). A multilevel Bayesian framework for predicting municipal waste generation rates. Waste Management, 127, 90-100.

Cui, H., Ou, Y., Wang, L., Yan, B., Li, Y., & Bao, M. (2021). Additive grain-size: An innovative perspective to investigate the transformation among heavy metal and phosphorus fractions during aerobic composting. Journal of Environmental Management, 292(May), 112768.

De Corato, U. (2020). Agricultural waste recycling in horticultural intensive farming systems by on-farm composting and compost-based tea application improves soil quality and plant health: A review under the perspective of a circular economy. Science of the Total Environment, 738, 139840.

Epelde, L., Jauregi, L., Urra, J., Ibarretxe, L., Romo, J., Goikoetxea, I., & Garbisu, C. (2018). Characterization of Composted Organic Amendments for Agricultural Use. Frontiers in Sustainable Food Systems, 2(July), 1-12.

Fetene, Y., Addis, T., Beyene, A., & Kloos, H. (2018). Valorisation of solid waste as key opportunity for green city development in the growing urban areas of the developing world. Journal of Environmental Chemical Engineering, 6(6), 7144-7151.

Gorai, P. S., Barman, S., Gond, S. K., & Mandal, N. C. (2020). Trichoderma. Beneficial Microbes in Agro-Ecology: Bacteria and Fungi, 571-591.

Gujre, N., Agnihotri, R., Rangan, L., Sharma, M. P. ., & Mitra, S. (2021). Deciphering the dynamics of glomalin and heavy metals in soils contaminated with hazardous municipal solid wastes. Journal of Hazardous Materials, 416(April), 125869.

Gujre, N., Mitra, S., Soni, A., Agnihotri, R., Rangan, L., Rene, E. R., & Sharma, M. P. (2021). Speciation, contamination, ecological and human health risks assessment of heavy metals in soils dumped with municipal solid wastes. Chemosphere, 262, 128013.

Hernández, D. J., Ferrera-Cerrato, R., & Alarcón, A. (2019). Trichoderma: Agricultural and biotechnological importance, and fermentation systems for producing biomass and enzymes of industrial interest. Chilean Journal of Agricultural and Animal Sciences, 35(1), 98-112.

Hernández, L., Benítez, M., & Bermúdez, J. (2018). Physical-chemical characterization of the organic fraction of urban solid waste from the controlled landfill at the Abel Santamaría Urban Center in Santiago de Cuba. Tecnología Química, 38(2), 369-379.

Hoornweg, D., & Bhada, P. (2012). What a Waste a Global Review of Solid Waste Management. Macrocognition Metrics and Scenarios: Design and Evaluation for Real-World Teams, 29-43.

Huang, G., Zhou, X., Guo, G., Ren, C., Rizwan, M. S., Islam, M. S., & Hu, H. (2020). Variations of dissolved organic matter and Cu fractions in rhizosphere soil induced by the root activities of castor bean. Chemosphere, 254, 126800.

INACAL. (2021). Norma Técnica Peruana del Instituto Nacional de Calidad, para Fertilizantes. Compost para uso agricola y requisitos. Primera Ed, 17.

Jalali, J., Magdich, S., Jarboui, R., Loungou, M., & Ammar, E. (2016). Phosphogypsum biotransformation by aerobic bacterial flora and isolated Trichoderma asperellum from Tunisian storage piles. Journal of Hazardous Materials, 308, 362-373.

Kaza, S., Shrikanth, S., & Chaudhary, S. (2021). More Growth, Less Garbage. More Growth, Less Garbage.

Křesinová, Z., Linhartová, L., Filipová, A., Ezechiáš, M., Mašín, P., & Cajthaml, T. (2018). Biodegradation of endocrine disruptors in urban wastewater using Pleurotus ostreatus bioreactor. New Biotechnology, 43, 53-61.

Kumar, A., Singhania, R. R., Albarico, F. P. J. B., Pandey, A., Chen, C. W., & Dong, C. Di. (2022). Organic wastes bioremediation and its changing prospects. Science of the Total Environment, 824, 153889.

Kumar, V., & Dwivedi, S. K. (2019). Hexavalent chromium stress response, reduction capability and bioremediation potential of Trichoderma sp. isolated from electroplating wastewater. Ecotoxicology and Environmental Safety, 185(September), 109734.

Lalas, S., Athanasiadis, V., & Dourtoglou, V. G. (2017). Humic and Fulvic Acids as Potentially Toxic Metal Reducing Agents in Water † Department of Food Technology , Technological Educational Institute of Thessaly , Karditsa , Department of Oenology & Beverage Technology , Technological Educational Institute of. November, 1-13.

Li, H., Wang, J., Zhao, B., Gao, M., Shi, W., et al. (2018). The role of major functional groups: Multi-evidence from the binding experiments of heavy metals on natural fulvic acids extracted from lake sediments. Ecotoxicology and Environmental Safety, 162(July), 514-520.

Liaquat, F., Haroon, U., Munis, M. F. H., Arif, S., Khizar, M., et al. (2021). Efficient recovery of metal tolerant fungi from the soil of industrial area and determination of their biosorption capacity. Environmental Technology and Innovation, 21.

Lipińska, A., Kucharski, J., & Wyszkowska, J. (2019). Activity of phosphatases in soil contaminated with PAHs. Water Air Soil Pollut, 230, 298.

Liu, H., Wu, M., Gao, H., Yi, N., & Duan, X. (2021). Hydrocarbon transformation pathways and soil organic carbon stability in the biostimulation of oil-contaminated soil: Implications of 13C natural abundance. Science of the Total Environment, 788, 147580.

Liu, Y., Ma, R., Tang, R., Kong, Y., Wang, J., Li, G., & Yuan, J. (2022). Effects of phosphate-containing additives and zeolite on maturity and heavy metal passivation during pig manure composting. Science of the Total Environment, 836(January), 155727.

López-Gómez, J. P., Latorre-Sánchez, M., Unger, P., Schneider, R., Coll Lozano, C., & Venus, J. (2019). Assessing the organic fraction of municipal solid wastes for the production of lactic acid. Biochemical Engineering Journal, 150(February), 107251.

Lopez-Ramirez, N., Volke-Sepulveda, T., Gaime-Perraud, I., Saucedo-Castañeda, G., & Favela-Torres, E. (2018). Effect of stirring on growth and cellulolytic enzymes production by Trichoderma harzianum in a novel bench-scale solid-state fermentation bioreactor. Bioresource Technology, 265(April), 291-298.

Ma, X. kui, l., Wu, L., & Fam, H. (2014). Heavy metal ions affecting the removal of polycyclic aromatic hydrocarbons by fungi with heavy-metal resistance. Applied Microbiology and Biotechnology, 98(23), 9817-9827.

Mahmoud, E., Ibrahim, M., Ali, N., & Ali, H. (2018). Spectroscopic analyses to study the effect of biochar and compost on dry mass of canola and heavy metal immobilization in soil. Communications in Soil Science and Plant Analysis, 49(16), 1990-2001.

Manna, M. C., Sahu, A., De, N., Thakur, J. K., Mandal, A., et al. (2020). Novel bio-filtration method for the removal of heavy metals from municipal solid waste. Environmental Technology and Innovation, 17.

Meena, M. D., Yadav, R. K., Narjary, B., Yadav, G., Jat, H. S., et al. (2019). Municipal solid waste (MSW): Strategies to improve salt affected soil sustainability: A review. Waste Management, 84, 38-53.

Mexicana, N. (2018). Dirección General de Normas -Norma Mexicana NMX-AA-180-SCFI-2018.

Mishra, S., Lin, Z., Pang, S., Zhang, Y., Bhatt, P., & Chen, S. (2021). Biosurfactant is a powerful tool for the bioremediation of heavy metals from contaminated soils. Journal of Hazardous Materials, 418(February), 126253.

Mudhoo, A., Ramasamy, D. L., Bhatnagar, A., Usman, M., & Sillanpää, M. (2020). An analysis of the versatility and effectiveness of composts for sequestering heavy metal ions, dyes and xenobiotics from soils and aqueous milieus. Ecotoxicology and Environmental Safety, 197(April), 110587.

NCh2880.c. (2003). Proyecto de Norma en Consulta Pública - Compost Clasificación y requisitos. Instituto Nacional de Normalización, 1-27.

Oshiquiri, L. H., dos Santos, K. R. A., Ferreira Junior, S. A., Steindorff, A. S., Barbosa Filho, J. R., et al. (2020). Trichoderma harzianum transcriptome in response to cadmium exposure. Fungal Genetics and Biology, 134, 103281.

Ozdemir, S., Turp, S. M., & Oz, N. (2020). Simultaneous dry-sorption of heavy metals by porous adsorbents during sludge composting. Environmental Engineering Research, 25(2), 258-265.

Paradelo, R., Villada, A., & Barral, M. T. (2020). Heavy metal uptake of lettuce and ryegrass from urban waste composts. International Journal of Environmental Research and Public Health, 17(8), 1-10.

Pérez, L., Salgado, I., Larrea, C., Martínez, A., Cruz, M., & Carballo, M. (2018). Biosorción microbiana de metales pesados: características del proceso. Cuban Journal of Biological Sciences, 6(1), 13.

Qu, C., Chen, W., Hu, X., Cai, P., Chen, C., Yu, X. Y., & Huang, Q. (2019). Heavy metal behaviour at mineral-organo interfaces: Mechanisms, modelling and influence factors. Environment International, 131, 104995.

Rahman, Z., & Singh, V. P. (2020). Bioremediation of toxic heavy metals (THMs) contaminated sites: concepts, applications and challenges. Environmental Science and Pollution Research, 27(22), 27563-27581.

Ramírez-Guzmán, K. N., De la Cruz-Quiroz, R., & Aguilar, C. N. (2016). Producción de Trichoderma harzianum y sus enzimas líticas por fermentación en medio sólido sobre residuos cítricos. Agronomía Colombiana, 34(1Supl), S1346-S1348.

Reyes-Pinto, K., Meza-Contreras, V., Alegre-Orihuela, J. C., & Réategui-Romero, W. (2020). Bioavailability and Solubility of Heavy Metals and Trace Elements during Composting of Cow Manure and Tree Litter. Applied and Environmental Soil Science, 2020.

Sala, A., Artola, A., Sánchez, A., & Barrena, R. (2020). Rice husk as a source for fungal biopesticide production by solid-state fermentation using B. bassiana and T. harzianum. Bioresource Technology, 296, 122322.

Sharma, P., Dutta, D., Udayan, A., Nadda, A. K., Lam, S. S., & Kumar, S. (2022). Role of microbes in bioaccumulation of heavy metals in municipal solid waste: Impacts on plant and human being. Environmental Pollution, 305, 1-15.

Sharma, S., Anand, G., Singh, N., & Kapoor, R. (2017). Arbuscular mycorrhiza augments arsenic tolerance in wheat (Triticum aestivum L.) by strengthening antioxidant defense system and thiol metabolism. Frontiers in Plant Science, 8(June), 1-21.

Song, C., Zhao, Y., Pan, D., Wang, S., Wu, D., et al. (2021). Heavy metals passivation driven by the interaction of organic fractions and functional bacteria during biochar/montmorillonite-amended composting. Bioresource Technology, 329(February).

Soobhany, N. (2018). Assessing the physicochemical properties and quality parameters during composting of different organic constituents of Municipal Solid Waste. Journal of Environmental Chemical Engineering, 6(2), 1979-1988.

Sowmya, S., Rekha, P. D., Yashodhara, I., Karunakara, N., & Arun, A. B. (2020). Uranium tolerant phosphate solubilizing bacteria isolated from Gogi, a proposed uranium mining site in South India. Applied Geochemistry, 114, 104523.

Sun, F. S., Yu, G. H., Ning, J. Y., Zhu, X. D., Goodman, B. A., & Wu, J. (2020). Biological removal of cadmium from biogas residues during vermicomposting, and the effect of earthworm hydrolysates on Trichoderma guizhouense sporulation. Bioresource Technology, 312(April), 123635.

Sun, H., Meng, M., Wu, L., Zheng, X., Zhu, Z., & Dai, S. (2020). Function and mechanism of polysaccharide on enhancing tolerance of Trichoderma asperellum under Pb2+ stress. International Journal of Biological Macromolecules, 151, 509-518.

Sun, J., Karuppiah, V., & Chen, J. (2020). The mechanism of heavy metal absorption and biodegradation of organophosphorus pesticides by Trichoderma. In New and Future Developments in Microbial Biotechnology and Bioengineering. Elsevier B.V.

Teng, Z., Shao, W., Zhang, K., Yu, F., Huo, Y., & Li, M. (2020). Enhanced passivation of lead with immobilized phosphate solubilizing bacteria beads loaded with biochar/ nanoscale zero valent iron composite. Journal of Hazardous Materials, 384, 121505.

Vallejo, M., Marín, M., Ramos, M., Silva, S., Ibarra, D., & Tamaris, J. (2021). Biosorción y tolerancia de Pb , Cr y Cd por la biomasa de Pleurotus Introducción. Revista Mexicana de Ciencias Agrícolas, 12(2), 275-289.

Vargas-García, M. del C., López, M. J., Suárez-Estrella, F., & Moreno, J. (2012). Compost as a source of microbial isolates for the bioremediation of heavy metals: In vitro selection. Science of the Total Environment, 431, 62-67.

Vázquez, M. B., Amodeo, M. R., & Bianchinotti, M. V. (2016). Estimación de la biomasa fúngica en un suelo del sudoeste de la provincia de Buenos Aires (Argentina) con una tinción directa con blanco de calcoflúor. Revista Argentina de Microbiologia, 48(3), 252-258.

Ventorino, V., Pascale, A., Fagnano, M., Adamo, P., Faraco, V., et al. (2019). Soil tillage and compost amendment promote bioremediation and biofertility of polluted area. Journal of Cleaner Production, 239(426), 118087.

Vullo, D. (2003). Microorganismos Y Metales Pesados: Una Interacción En Beneficio Del Medio Ambiente. Química Viva, 2(3), 93-104.

Wan, L., Wang, X., Cong, C., Li, J., Xu, Y., et al. (2020). Effect of inoculating microorganisms in chicken manure composting with maize straw. Bioresource Technology, 301, 122730.

Wang, L., Liu, H., Prasher, S. O., Ou, Y., Yan, B., & Zhong, R. (2021). Effect of inorganic additives (rock phosphate, PR and boron waste, BW) on the passivation of Cu, Zn during pig manure composting. Journal of Environmental Management, 285(February), 112101.

Wang, M., Liu, Y., Wang, S., Wang, K., & Zhang, Y. (2021). Development of a compound microbial agent beneficial to the composting of Chinese medicinal herbal residues. Bioresource Technology, 330(January), 124948.

Wei, Y., Zhao, Y., Zhao, X., Gao, X., Zheng, Y., Zuo, H., & Wei, Z. (2020). Roles of different humin and heavy-metal resistant bacteria from composting on heavy metal removal. Bioresource Technology, 296.

Wolna-Maruwka, A., Dach, J., Rafaela, C., Czekała, W., Niewiadomska, A., Janczak, D., & Budka, A. (2019). An effective method of utilizing vegetable waste in the form of carriers for Trichoderma strains with phytosanitary properties. Science of the Total Environment, 671, 795-804.

Xiong, R., Gao, X., Tu, X., Mao, Y., Jiang, L., Zheng, L., & Du, Y. (2022). Heavy metal remediation in sludge compost: Recent progress. Journal of Renewable Materials, 10(2), 469-486.

Yazid, N. A., Barrena, R., Komilis, D., & Sánchez, A. (2017). Solid-state fermentation as a novel paradigm for organic waste valorization: A review. Sustainability (Switzerland), 9(2), 1-28.

Yin, K., Wang, Q., Lv, M., & Chen, L. (2019). Microorganism remediation strategies towards heavy metals. Chemical Engineering Journal, 360(October), 1553-1563.

Yu, M., He, X., Liu, J., Wang, Y., Xi, B., et al. (2018). Characterization of isolated fractions of dissolved organic matter derived from municipal solid waste compost. Science of the Total Environment, 635, 275-283.

Yuksel, O. (2015). Influence of municipal solid waste compost application on heavy metal content in soil. Environmental Monitoring and Assessment, 187(6).

Zhang, H., Yuan, X., Xiong, T., Wang, H., & Jiang, L. (2020). Bioremediation of co-contaminated soil with heavy metals and pesticides: Influence factors, mechanisms and evaluation methods. Chemical Engineering Journal, 398.

Zhou, S., Kong, F., Lu, L., Wang, P., & Jiang, Z. (2022). Biochar — An effective additive for improving quality and reducing ecological risk of compost: A global meta-analysis. Science of the Total Environment, 806, 151439.