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Characterization and evaluation of the bioremediation potential of Rhizopus microsporus Os4 isolated from arsenic-contaminated soil

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Abstract

The persistent presence of arsenic (As) pollution in soils worldwide poses a significant threat to human and environmental health, highlighting the urgent need for effective remediation strategies. Therefore, this study aims to evaluate the capacity of the Rhizopus microsporus Os4 fungal strain, to remove As from contaminated media in laboratory studies. R. microsporus Os4 was isolated from soils of a recreation area of Concepción del Oro, Zacatecas, México, where As concentrations ranged from 146.56 to 11,233.81 mg Kg−1. Os4 was grown in a culture medium with arsenic V (As(V)), and strain resistance was determined at concentrations up to 15,000 mg L−1. In removal assays using a liquid medium with 7,000 mg L−1, Os4 was capable of reducing 90% of the As(V) concentration after 7 days. To determine whether arsenic has an impact on fungal cell walls, Fourier Transform Infrared Spectroscopy analysis was performed, confirming the presence of functional groups in mycelium cell walls with the ability to facilitate the biosorption of arsenic mycelium cell walls. Scanning Electron Microscopy confirmed surface damage and cell morphology changes a response to cell stress induced by contact with As(V). These findings indicate that R. microsporus Os4 employs a biosorption mechanism on the cell wall for arsenic removal, suggesting its potential application in the bioremediation of arsenic-contaminated soils.

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Data availability

The authors declare that the data supporting the findings of this study are available within the paper. Should any raw data files be needed in another format they are available from the corresponding author upon reasonable request. Source data are provided with this paper.

References

  • Abbas, S. H., Ismail, I. M., Mostafa, T. M., & Sulaymon, A. H. (2014). Biosorption of heavy metals: A review. Journal of Chemical Science and Technology, 3(4), 74–102.

    Google Scholar 

  • Alcalá-Jáuregui, J. A., Rodríguez-Ortiz, J. C., Hernández-Montoya, A., Villarreal-Guerrero, F., Cabrera-Rodríguez, A., Beltran-Morales, F. A., & Díaz Flores, P. E. (2014). Heavy metal contamination in sediments of a riparian area in San Luis Potosi, Mexico. Revista de la Facultad de Ciencias Agrarias. Universidad Nacional de Cuyo. Mendoza. Argentina., 46(2), 203–221.

    Google Scholar 

  • Aljanabi, S. M., & Martinez, I. (1997). Universal and rapid salt-extraction of high-quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 25(22), 4692–4693. https://doi.org/10.1093/nar/25.22.4692

    Article  CAS  Google Scholar 

  • APHA, Awwa, and WPCF. (1998). Standard Methods for the Examination of Water and Wastewater. American Public Health Association.

    Google Scholar 

  • Asere, T. G., Stevens, C. V., & Du Laing, G. (2019). Use of (modified) natural adsorbents for arsenic remediation: A review. Science of the Total Environment, 676, 706–720. https://doi.org/10.1016/j.scitotenv.2019.04.237

    Article  CAS  Google Scholar 

  • Bastidas, O. (2011). Cell counting with hematocytometer: Elementary use of the hematocytometer. San Francisco, CA, USA. https://www.scribd.com/document/105937668/Conteo-Camara-Neubauer. (consulted, October 19th, 2023)

  • Cano-Ruera. (2006). Métodos de análisis microbiológico. Normas ISO. UNE. ANALIZA Calidad: España. Retrieved February 6, 2023, from https://www.academia.edu/3626555/An%C3%A1lisis_microbiol%C3%B3gicos

  • Canonica, L., Cecchi, G., Capra, V., Di Piazza, S., Girelli, A., Zappatore, S., & Zotti, M. (2024). Fungal Arsenic Tolerance and Bioaccumulation: Local Strains from Polluted Water vs. Allochthonous Strains. Environments, 11(1), 23. https://doi.org/10.3390/environments11010023

    Article  Google Scholar 

  • El-Sayed, W., & Hurle, K. (2001). Efficacy of Phomopsis convolvulus as a mycoherbicide for Convolvulus arvensis. Communications in Agricultural and Applied Biological Sciences, 66, 775–790.

    CAS  Google Scholar 

  • El-Sayed, M. T. (2015). An investigation on tolerance and biosorption potential of Aspergillus awamori ZU JQ 965830.1 TO Cd (II). Annals of Microbiology., 65(1), 69–83. https://doi.org/10.21608/ejm.2013.246

    Article  CAS  Google Scholar 

  • Ezzouhri, L., Castro, E., Moya, M., Espinola, F., & Lairini, K. (2009). Heavy metal tolerance of filamentous fungi isolated from polluted sites in Tangier. Morocco. Journal of Microbiology Research, 3(2), 35–48.

    CAS  Google Scholar 

  • Fernández, P. M., Viñarta, S. C., Bernal, A. R., Cruz, E. L., & Figueroa, L. I. (2018). Bioremediation strategies for chromium removal: Current research, scale-up approach and future perspectives. Chemosphere, 208, 139–148. https://doi.org/10.1016/j.chemosphere.2018.05.166

    Article  CAS  Google Scholar 

  • Grimm, A., Zanzi, R., Björnbom, E., & Cukierman, A. L. (2008). Comparison of different types of biomasses for copper biosorption. Bioresource Technology, 99(7), 2559–2565. https://doi.org/10.1016/j.biortech.2007.04.036

    Article  CAS  Google Scholar 

  • Halling, R. E. (2005). Biodiversity of Fungi: Inventory and Monitoring Methods. Economic Botany, 59(1), 87–87.

    Article  Google Scholar 

  • Harley, M., & Ferguson, I. K. (1990). The role of SEM in pollen morphology and plant systematics (pp. 45–68). Oxford University Press.

    Google Scholar 

  • Hyde, K. D., Xu, J., Rapior, S., Jeewon, R., Lumyong, S., Niego, A. G. T., & Stadler, M. (2019). El asombroso potencial de los hongos: 50 formas en que podemos explotar los hongos industrialmente. Diversidad De Hongos, 97, 1–136. https://doi.org/10.1007/s13225-019-00430-9

    Article  Google Scholar 

  • Kapahi, M., & Sachdeva, S. (2019). Bioremediation options for heavy metal pollution. Journal of Health and Pollution, 9(24). https://doi.org/10.5696/2F2156-9614-9.24.191203

  • Kumar, M., Bolan, N., Zad, T. J., Padhye, L., Sridharan, S., Singh, L., & Rinklebe, J. (2022). Mobilization of contaminants: Potential for soil remediation and unintended consequences. Science of the Total Environment, 839, 156373. https://doi.org/10.1016/j.scitotenv.2022.156373

    Article  CAS  Google Scholar 

  • Latha, J. N. L., Babu, P. N., Rakesh, P., Kumar, K. A., Anupama, M., & Susheela, L. (2012). Fungal cell walls as protective barriers for toxic metals. Advances in Medicine and Biology, 53, 181–198. ISBN:978-1-62081-565-6.

    Google Scholar 

  • Liang, J., Diao, H., Song, W., & Li, L. (2018). Tolerance and bioaccumulation of arsenate by Aspergillus oryzae TLWK-09 isolated from arsenic-contaminated soils. Water, Air, & Soil Pollution, 229(5), 169. https://doi.org/10.1007/s11270-018-3822-1

    Article  CAS  Google Scholar 

  • Litter, M. I., Ingallinella, A. M., Olmos, V., Savio, M., Difeo, G., Botto, L., & Ahmad, A. (2019). Arsenic in Argentina: Occurrence, human health, legislation, and determination. Science of the Total Environment, 676, 756–766. https://doi.org/10.1016/j.scitotenv.2019.04.262

    Article  CAS  Google Scholar 

  • NMX-AA-132-SCFI-2006. (2006). Muestreo de suelos para la identificación y la cuantificación de metales y metaloides, y manejo de la muestra. Publicada en el Diario Oficial de la Federación.

    Google Scholar 

  • Norma Oficial Mexicana NOM-021-RECNAT-2000. (2000). Que establece las especificaciones de fertilidad, salinidad y clasificación de suelos. Estudios, muestreo y análisis (2ª Ed 2002). Diario Oficial de la Federación.

    Google Scholar 

  • Norma Oficial Mexicana NOM-147-SEMARNAT-SSA1–2004. (2004). Norma Oficial Mexicana que establece criterios para determinar las concentraciones de remediación de suelos contaminados por arsénico, bario, berilio, cadmio, cromo hexavalente, mercurio, plomo, plata, selenio, talio y/o vanadio (2 Ed, 2007). Diario Oficial de la Federación.

    Google Scholar 

  • 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, 29–37. https://doi.org/10.1016/j.bjm.2017.06.003

    Article  CAS  Google Scholar 

  • Pacasa-Quisbert, F. (2017). Micología en Bolivia: Un tema latente. Journal of the Selva Andina Research Society, 8(1), 1–1. (in Spanish).

    Article  Google Scholar 

  • Pei, Q. H., Shahir, S., Raj, A. S., Zakaria, Z. A., & Ahmad, W. A. (2009). Chromium (VI) resistance and removal by Acinetobacter haemolyticus. World Journal of Microbiology and Biotechnology, 25(6), 1085–1093. https://doi.org/10.1007/s11274-009-9989-2

    Article  CAS  Google Scholar 

  • Prasad, K. S., Ramanathan, A. L., Paul, J., Subramanian, V., & Prasad, R. (2013). Biosorption of arsenite (As+3) and arsenate (As+5) from aqueous solution by Arthrobacter sp. biomass. Environmental Technology, 34(19), 2701–2708. https://doi.org/10.1080/09593330.2013.786137

    Article  CAS  Google Scholar 

  • Priyadarshanee, M., & Das, S. (2021). Biosorption and removal of toxic heavy metals by metal tolerating bacteria for bioremediation of metal contamination: A comprehensive review. Journal of Environmental Chemical Engineering, 9(1), 104686. https://doi.org/10.1016/j.jece.2020.104686

    Article  CAS  Google Scholar 

  • Rathi, B. S., & Kumar, P. S. (2021). A review on sources, identification, and treatment strategies for the removal of toxic Arsenic from water system. Journal of Hazardous Materials, 418, 126299. https://doi.org/10.1016/j.jhazmat.2021.126299

    Article  CAS  Google Scholar 

  • Romero, D. D., Rivera, H. V., Reyes, B. R., Reyes, J. A., & Campos, A. M. (2013). Aislamiento y Purificación del Hongo Ectomicorrízico Helvella Lacunosa en diferentes medios de cultivo. Tropical and Subtropical Agroecosystems, 16(1), 51–59. http://hdl.handle.net/20.500.11799/39971.

    Google Scholar 

  • Rosa, E., Di Piazza, S., Cecchi, G., Mazzoccoli, M., Zerbini, M., Cardinale, A. M., & Zotti, M. (2022). Applied Tests to Select the Most Suitable Fungal Strain for the Recovery of Critical Raw Materials from Electronic Waste Powder. Recycling, 7(5), 72. https://doi.org/10.3390/recycling7050072

    Article  Google Scholar 

  • Shahid, M., Khalid, S., Abbas, G., Shahid, N., Nadeem, M., Sabir, M. & Dumat, C. (2015). Heavy metal stress and crop productivity. Crop production and global environmental issues. 1–25. https://doi.org/10.1007/978-3-319-23162-4_1.

  • Shinde, B., Berge, S., Jadhav, T., Magdum, P., & Sharma, R. (2021). Screening of Secondary Metabolites Produced by Streptomyces Species from a Soil Sample that Can Produce Anti-Nematodal and Antiprotozoal Avermectins. Journal of Pharmaceutical Research International, 33(6), 90–98. https://doi.org/10.9734/jpri/2021/v33i631192

    Article  CAS  Google Scholar 

  • Singh, R., Singh, S., Parihar, P., Singh, V. P., & Prasad, S. M. (2015). Arsenic contamination, consequences, and remediation techniques: A review. Ecotoxicology and Environmental Safety, 112, 247–270. https://doi.org/10.1016/j.ecoenv.2014.10.009

    Article  CAS  Google Scholar 

  • Solis-Pareja, C. (2020). Estrategias basadas en producción más limpia y biorremediación para mitigar los impactos ambientales negativos generados por los efluentes industriales de las curtiembres del parque industrial de Río Seco, Arequipa. Dissertation. Universidad Nacional de San Agustín de Arequipa.

    Google Scholar 

  • Song, W., Liang, J., Wen, T., Wang, X., Hu, J., Hayat, T., & Wang, X. (2016). Accumulation of Co (II) and Eu (III) by the mycelia of Aspergillus niger isolated from radionuclide-contaminated soils. Biochemical Engineering Journal, 304, 186–193. https://doi.org/10.1016/j.cej.2016.06.103

    Article  CAS  Google Scholar 

  • Soto, J., Ortiz, J., Herrera, H., Fuentes, A., Almonacid, L., Charles, T. C., & Arriagada, C. (2019). Enhanced arsenic tolerance in Triticum aestivum inoculated with arsenic-resistant and plant growth promoter microorganisms from a heavy metal-polluted soil. Microorganisms, 7(9), 348. https://doi.org/10.3390/microorganisms7090348

    Article  CAS  Google Scholar 

  • Sun, J., Zou, X., Ning, Z., Sun, M., Peng, J., & **ao, T. (2012). Culturable microbial groups and thallium-tolerant fungi in soils with high thallium contamination. Science of the Total Environment, 441, 258–264. https://doi.org/10.1016/j.scitotenv.2012.09.053

    Article  CAS  Google Scholar 

  • Wang, J., & Chen, C. (2006). Biosorption of heavy metals by Saccharomyces cerevisiae: A review. Biotechnology Advances, 24(5), 427–451. https://doi.org/10.1016/j.biotechadv.2006.03.001

    Article  CAS  Google Scholar 

  • White, T. J., Bruns, T., Lee, S. J. W. T., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications, 18(1), 315–322.

    Google Scholar 

  • WHO - World Health Organization. (2003). Arsenic in drinking-water: background document for development of WHO guidelines for drinking-water quality (No. WHO/SDE/WSH/03.04/75).

    Google Scholar 

  • Wondimu, T. (2018). Chemical Speciation Of Essential Metal Ion Complexes Of L-Phenylalanine And Maleic Acid. Dimethylormamide-Water Mixture. Dissertation. ASTU.

    Google Scholar 

  • Yin, K., Wang, Q., Lv, M., & Chen, L. (2019). Microorganism remediation strategies towards heavy metals. Biochemical Engineering Journal, 360, 1553–1563. https://doi.org/10.1016/j.cej.2018.10.226

    Article  CAS  Google Scholar 

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Acknowledgements

We gratefully acknowledge the support of the National Council of Humanities Sciences and Technologies (Consejo Nacional de Humanidades Ciencias y Tecnologías) Mexico, by means of the research scholarship #467195 used in part for this study.

Funding

This work was financially supported by the Universidad Autónoma de Aguascalientes (UAA) through the project number PIT 19-3, Aguascalientes, México.

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Authors and Affiliations

  1. Universidad Autónoma de Aguascalientes, Avenida Universidad #940, 2023, Aguascalientes, Ags., México

    Oscar Abraham Flores-Amaro, Magdalena Samanta Ramos-Gómez, Alma Lilian Guerrero-Barrera, Laura Yamamoto-Flores & Francisco Javier Avelar-González

  2. Instituto Tecnológico de Pabellón de Arteaga, Carretera a la estación de Rincón de Romos, Km. 1, 20,670, Pabellón de Arteaga, Ags., México

    Pamela Romo-Rodríguez

  3. St. George’s University, True Blue, P. O. Box 7, St. George’s, Grenada

    Kerry Mitchell

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  1. Oscar Abraham Flores-Amaro
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Correspondence to Francisco Javier Avelar-González.

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Flores-Amaro, O., Ramos-Gómez, M., Guerrero-Barrera, A. et al. Characterization and evaluation of the bioremediation potential of Rhizopus microsporus Os4 isolated from arsenic-contaminated soil. Water Air Soil Pollut 235, 529 (2024). https://doi.org/10.1007/s11270-024-07232-z

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