Isolation and selection of Glyphosate herbicide tolerant fungi
DOI:
https://doi.org/10.33448/rsd-v11i1.24782Keywords:
Bioremediation; Phenoloxidases; Xenobiotics; Herbicides.Abstract
The objective of this work was to isolate fungi from an ecological reserve in the Brazilian Midwest and to select species tolerant to glyphosate, a herbicide widely used in agriculture. The purified isolates were subjected to qualitative tests to assess the oxidizing capacity of gallic acid and RBBR dye discoloration. Then, the selected fungi were identified through molecular biology techniques and used in herbicide tolerance tests. Fungal growth rates (FG) and fungal growth inhibition (FGI) in the absence and presence of different concentrations of glyphosate (10 mg mL-1, 30 mg mL-1 and 50 mg mL-1) were evaluated. For statistical analysis, a double factorial scheme (fungus and concentration) was used, followed by the Tukey test (p ≤ 0.05). A total of 44 fungi were isolated in the field, having a purification efficiency of 50%. Of these, 60% showed positive results in the gallic acid test and 45.5% were positive for RBBR discoloration. The seven fungi selected from the qualitative tests were tolerant to the herbicide glyphosate, with Phanerochaete australis SA18 standing out with higher FG, lower FGI and mycelial growth significantly higher compared to other fungi in all tests. Thus, the use of P. australis SA18 is recommended for further studies on the production of ligninolytic enzymes, degradation and production of glyphosate metabolites and tests on bioremediation of contaminated agricultural soils.
References
Adelowo, F. E., Olu-Arotiowa, O. A., & Amuda, O. S. (2014). Biodegradation of Glyphosate by Fungi Species. Advances in Bioscience and Bioengineering, 104-118. https://www.semanticscholar.org/paper/Biodegradation-of-Glyphosate-by-Fungi-Species-Adelowo-Olu-arotiowa/b6823c1f061b431ffbbed8628 1f0f5f86e dc9dbd?sort=rele vance&citationIntent=methodology
Amazonas, M. A. L. A. (2003). Biodiversidade de macrofungos e potencial de uso para o desenvolvimento sustentável. Embrapa Florestas. https://www.embrapa.br/busca-de-publicacoes/-/publicacao/308602/biodiversidade-de-macrofungos-e-potencial-de-uso-para-o-desenvolvimento-sustentavel.
Ambiente Brasil. (n.d.). https://ambientes.ambientebrasil.com.br/unidades_de_conservacao/estacao_ecologica/estacao_ecologica_serra_das_araras.html.
Araújo, A. S. F. (2002) Biodegradação, extração e análise de glifosato em dois tipos de solos [Dissertação de Mestrado, Universidade de São Paulo]. https://doi.org/10.11606/D.11.2002.tde-05092002-161341
Arfarita, N., Imai, T., & Prasetya, V. (2014). Potential use of soil-born fungi isolated from treated soil in Indonesia to degrade glyphosate herbicide. Journal of Degraded and Mining Lands Management, 63-68. https://jdmlm.ub.ac.id/index.php/jdmlm/article/view/28. DOI: 10.15243/jdmlm.2014.012.063.
Argumedo-delira, R., Alarcon, A., Ferrera-Cerrato, R., Almaraz, J. J., & Peña-Cabriales, J. J. (2012). Tolerance and growth of 11 Trichoderma strains to crude oil, naphthalene, phenanthrene and benzo[a]pyrene. Journal of Environmental Management, v. 95, n. SUPPL., p. S291–S299. https://doi.org/10.1016/j.jenvman.2010.08.011
Barbosa, V. F. (2010). Caracterização do perfil da ação do ácido gálico e seus derivados sobre processos oxidativos in vitro e ex vivo [Dissertação de Mestrado Universidade Estadual Paulista]. https://repositorio.unesp.br/handle/11449/87981
Barroso, A. A. M., & Murata, A. T. (2021). Matologia: estudos sobre plantas daninhas (1º ed.). Fábrica de Palavras.
Benbrook, C. M. (2019). How did the US EPA and IARC reach diametrically opposed conclusions on the genotoxicity of glyphosate-based herbicides? Environmental Science Europe. https://doi.org/10.1186/s12302-018-0184-7.
Berlinck, R. G. S. (2012). Bioprospecção no Brasil: um breve histórico. Ciência e Cultura. http://dx.doi.org/10.21800/S0009-67252012000300010
Bononi, V. L. R., Machado, K. M. G., Matheus, D. R., & Vitali, V. M. (2008). Biodegradação de organoclorados no solo por basidiomicetos lignocelulolíticos. In: Melo, I. S., Azevedo, J. L. Microbiologia Ambiental. Embrapa Meio Ambiente.
Carranza, C. S., Barberis, C. L., Chiacchiera, S. M., & Magnoli, C. E. (2017). Assessment of growth of Aspergillus spp. from agricultural soils in the presence of glyphosate. Rev Argent Microbiol, 384–393. https://doi.org/10.1016/j.ram.2016.11.007
Castellani, A. (1939). Viability of some pathogenic fungi in distilled water. Journal of Tropical Medicine and Hygiene, 225-226.
Castro júnior, J. V., Selbach, P. A., & Záchaayub, M. A. (2006). Avaliação do efeito do herbicida glifosato na microbiota do solo. Pesticidas: Revista de Ecotoxicologia e Meio Ambiente, 21-30. https://revistas.ufpr.br/pesticidas/article/view/7476/5345
Catarino, S. R. M. (2016). Biorremediação [Monografia de Mestrado Universidade de Coimbra]. https://estudogeral.uc.pt/bitstream/10316/41900/2/Monografia%203.pdf
Colla, L. M., Primaz, A. L., Lima, M., Bertolin, T. E., & Costa, J. A. V. (2008). Isolamento e seleção de fungos para biorremediação a partir de solo contaminado com herbicidas triazínicos. Ciências e Agrotecnologia, 809-813. https://doi.org/10.1590/S1413-70542008000300016
Correa, L. O., Bezerra, A. F. M., Honorato, L. R. S., Cortez, A. C. A., Souza, J. V. B., & Souza, E. S. Amazonian soil fungi are efficient degraders of glyphosate herbicide, novel isolates of Penicillium, Aspergillus, and Trichoderma. Brazilian Journal of Biology. https://doi.org/10.1590/1519-6984.242830
Davidson, W. R., Campbell, W. A., & Baisdell, D. J. (1938). Differentiations of wood-decaying fungy by their reactions on gallic or tanic acid medium. Journal of Agricultural Research, 683-695. https://naldc.nal.usda.gov/download/IND43969196/PDF
Eman, A., Sadik, M.W., Abdel-Megeed, A., Suliman, A., & Sholkamy, E. N. (2013). Biodegradation of Glyphosate by Fungal Strains Isolated from Herbicides Polluted-Soils in Riyadh Area. British Journal of Environmental Sciences, 7-29. https://www.eajournals.org/journals/british-journal-of-environmental-sciences-bjes/vol-1-issue-1-december-2013/biodegradation-glyphosate-fungal-strains-isolated-herbicides-polluted-soils-riyadh-area/
Filho, S. A, Silva, C. G. N., & Bigi, M. F. M. A. (2014). Bioprospecção e biotecnologia. Parcerias Estratégicas. Brasília-DF, v. 19, n. 38, p. 45-80, 2014. Disponível em: http://seer.cgee.org.br/index.php/parcerias_estrategicas/article/viewFile/732/672
Forlani, G., Mangiagalli, A., Nielsen, E., & Suardi, C. M. (1999). Degradation of the phosphonate herbicide glyphosate in soil: evidence for a possible involvement of unculturable microorganisms. Soil Biology and Biochemistry, 991-997. https://doi.org/10.1016/S0038-0717(99)00010-3
Gaylarde, C. C., Bellinaso, M. D. L., & Manfio, G. P. (2005). Biorremediação: Aspectos Biológicos e Técnicos da Biorremediação de Xenobióticos. Biotecnologia, Ciência e Desenvolvimento, p. 36–43. https://edisciplinas.usp.br/pluginfile.php/4144372/mod_resource/content/1/Biorremediac%CC%A7a%CC%83o%20-%20Artigo%201.pdf
Glass, N. L., & Donaldson, G. (1995). Development of primer sets designed for use with PCR to amplify conserved genes from filamentous ascomycetes. Applied Environmetal Microbiology, 1323-1330. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC167388/
Guerrero, R. T., & Homrich, M. H. (1999). Fungos Macroscópicos comuns no Rio Grande do Sul (2nd ed.). Universidade/UFRGS.
Harms, H., Schlosser, D., & Wick, L. Y. (2011). Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nature Reviews Microbiology, 177-192. https://doi.org/10.1038/nrmicro2519
Hough, R. L. A world view of pesticides. Nature Geoscience, 14, 183–184. https://doi.org/10.1038/s41561-021-00723-2
Javaid, M. K., Ashiq, M., & Tahir, M. (2016). Potential of biological agents in decontamination of agricultural soil. Scientifca. https://doi.org/10.1155/2016/1598325.
Katoh, K.., & Toh, H. (2008). Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics, 86-98. http://dx.doi.org/10.1093/bib/bbn013
Kim, Y-J. (2007). Antimelanogenic and antioxidant properties of gallic acid. Biological and Pharmaceutical Bulletin, 1052-1055. https://doi.org/10.1248/bpb.30.1052
Landrigan, P., & Belpoggi, F. (2018). The need for independent research on the health effects of glyphosate-based herbicides. Environmental Health. https://doi.org/10.1186/s12940-018-0392-z
Lee, A.H., Lee, H., Heo, Y.M., Lim,Y. W., Kim, C., Kim, G., Chang, W., & Kim, J. (2020). A proposed stepwise screening framework for the selection of polycyclic aromatic hydrocarbon (PAH)-degrading white rot fungi. Bioprocess Biosyst Eng, 767–783. https://doi.org/10.1007/s00449-019-02272-w
Lee, H., Jang, Y., Choi, Y., Kim, M., Lee, J., Lee, H., Hong, J., Lee, Y. M., Kim, G., & Kim, J. (2014). Biotechnological procedures to select white rot fungi for the degradation of PAHs. Journal of Microbiological Methods, 56–62. https://doi.org/10.1016/j.mimet.2013.12.007
Lenhard, D. C. (2006). Descoloração de corantes têxteis reativos por fungos ligninolíticos e por lacase [Dissertação de Mestrado, Universidade Estadual de Maringá]. http://www.dominiopublico.gov.br/pesquisa/DetalheObraForm.do?select_action=&co_obra=157422
Maggi, F., Cecilia, D., Tang, F. H. M., & McBratney, A. (2020). The global environmental hazard of glyphosate use. Science of the Total Environment. https://doi.org/10.1016/j.scitotenv.2020.137167
Mahmood I., Imadi S.R., Shazadi K., Gul A., & Hakeem K. R. (2016). Effects of Pesticides on Environment. Plant, Soil and Microbes. https://doi.org/10.1007/978-3-319-27455-3_13
Malty, J. S., siqueira, J. O., & Moreira, F. M. S. (2006). Efeitos do glifosato sobre microrganismos simbiotróficos de soja, em meio de cultura e casa de vegetação. Pesquisa Agropecuária Brasileira, 285-291. https://doi.org/10.1590/S0100-204X2006000200013
Monteiro, P. H. R. et al. (2012). Estudo sobre a viabilidade de remediação de pesticidas por ectomicorrizas e avaliação da sua tolerância em exposição ao glifosato. A responsabilidade socioambiental da pesquisa agrícola. https://www.alice.cnptia.embrapa.br/alice/handle/doc/934518
Moraes, P. V. D., & Rossi, P. (2010). Comportamento ambiental do glifosato. Scientia Agraria Paranaensis, 22-35. http://e-revista.unioeste.br/index.php/scientiaagraria/article/view/5258
Nyakundi, W. O., Magoma, G., Ochora, J., & Nyende, A. B. (2011). Biodegradation of diazinon and methomyl pesticides by whiterot fungi from selected horticultural farms in rift valley and central kenya. Journal of Applied Technology in Environmental Sanitation, 107–124. http://ir.jkuat.ac.ke/bitstream/handle/123456789/948/BIODEGRADATION%20OF%20DIAZINON%20AND%20METHOMYL%20PESTICIDES%20BY%20WHITE.pdf?sequence=1&isAllowed=y
Nylander, J. A. A. MrModeltest Version 2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala, 2004. https://www.researchgate.net/publication/285805344_MrModeltest_V2_Program_Distributed_by_the_Author
O’donnell, K., & Cigelnik, E. (1997). Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Molecular Phylogenetics and Evolution, 103-116. https://doi.org/10.1006/mpev.1996.0376
Peillexa, C., & Pelletier, M. (2020). The impact and toxicity of glyphosate and glyphosate-based herbicides on health and immunity. Journal of Immunotoxicology, 163-174. https://doi.org/10.1080/1547691X.2020.1804492.
Pietrobon, C. B., & Senem, J. V. (2015). Avaliação dos efeitos toxicológicos do herbicida glifosato sore o estomago de ratos Wistar machos. Revista Cultivando o Saber, 172-183. https://www.fag.edu.br/upload/revista/cultivando_o_saber/55d1eed313659.pdf
Pizzul, L., Castillo, M. P., & Stenstrom, J. (2009). Degradation of glyphosate and other pesticides by ligninolytic enzymes. Biodegradation,751–759. DOI 10.1007/s10532-009-9263-1.
Rainert, K. T., Chicatto, J. L., Gonçalves, M. J., Vaz, D. A., & Tavares, L. B. B. (2016). Adisorção do corante Reactive Blue 19 por bainha do palmito Pupunha in natura. IV Congresso cientifico têxtil e moda-CONTEXMOD. http://www.contexmod.net.br/index.php/quarto/article/view/425
Rambaut, A. FigTree version 1.3.1. (computer program), 2009. http://tree.bio.ed.ac.uk/software/figtree/. Acesso em: 17 fev. 2021.
Rehner, S. A., & Samuels, G. J. (1994). Taxonomy and phylogeny of Gliocladium analysed from nuclear large subunit ribosomal DNA sequences. Mycological Research, 625-634. https://doi.org/10.1016/S0953-7562(09)80409-7
Rodriguez, J. P. G. (2014). Identificação dos compostos produzidos na degradação do corante Remazol Brilliant Blue R (RBBR) pela ação do fungo do ambiente marinho Tinctoporellus [Dissertação de Mestrado, Universidade de São Paulo]. https://teses.usp.br/teses/disponiveis/75/75135/tde-10062014-104028/pt-br.php
Ronquist, F., Teslenko, M., Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 539-542. https://doi.org/10.1093/sysbio/sys029
Saccaro Júnior, N. L. (2011). Desafios da bioprospecção no Brasil. Instituto de Pesquisa Econômica Aplicada-IPEA. https://www.ipea.gov.br/portal/index.php?option=com_content&view=article&id=7066
Santana, M. D. F. Rodrigues, L. S. I., Amaral, T. S., & Pinheiro, Y. G. (2016). Fenoloxidases e biodegradação do corante têxtil azul brilhante blue r (RBBR) para três espécies de macrofungos coletados na Amazônia. SasBios: Revista de Saúde e Biologia, 53-60. https://tratamentodeagua.com.br/wp-content/uploads/2017/04/fenoloxidase-e-biodegradacao-corante-textil-azul-brilhante-de-remazol-r-rbbr-para-tres-especies-de-macrofungos-coletadas-na-amazonia.pdf
Singh, S., Kumar, V., Datta, S., Wani, A. B., Dhanjal, D. S., Romero, R., & Singh, J. (2020a). Glyphosate uptake, translocation, resistance emergence in crops, analytical monitoring, toxicity and degradation: a review. Environ Chem Lett, 663–702. https://doi.org/10.1007/s10311-020-00969-z
Singh, S., Kumar, V., Gill, J.P.K., Datta, S., Singh, S., Dhaka, V., Kapoor, D., Wani, A.B., Dhanjal, D.S., Kumar, M., Harikumar, S.L., & Singh, J. (2020b). Herbicide Glyphosate: Toxicity and Microbial Degradation. Int J Environ Res Public Health. doi: 10.3390/ijerph17207519
Souza, H. M. L., Sette, L. D., Mota, A. J., Neto, J. F. N., Rodrigues, R., Oliveira, T. B., Oliveira, F. M., Oliveira, L. A., Barroso, H. S., & Zanotto, S. P. (2016). Filamentous fungi isolates of contaminated sediment in the amazon region with the potential for benzo(a)pyrene degradation. Water, Air, & Soil Pollution. https://doi.org/10.1007/s11270-016-3101-y
Souza, H. M. de L., Barreto, L. R., Mota, A. J. da, Oliveira, L. A. de, Barroso, H. dos S., & Zanotto, S. P. (2017). https://doi.org/10.4025/actascibiolsci.v39i4.34709
Vacondio, B., Birolli, w. G., Seleghim, M. H. R., Gonçalvez, S., Vasconcellos, S. P., & Porto, A. L. M. (2015). Screening of Marine-derived Fungi Isolated from the sponge Didemnun ligulum for Biodegradation of Pentachlorophenol. Advances in Bioremediation of Wastewater and Polluted Soil, 193-225. http://dx.doi.org/10.5772/60777
Vilgalys, R., & Hester, M. (1990). Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology, 4239-4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990
White, T. J., Bruns, T., & Taylor, J. (1990). Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. Academic Press, 315-322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Zhan, H., Feng, Y., Fan, X. & Chen, S. (2018). Recent advances in glyphosate biodegradation. Applied Microbiology and Biotechnology, https://doi.org/10.1007/s00253-018-9035-0
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 Felipe Soares de Souza; Hilton Marcelo de Lima Souza; João Arthur dos Santos Oliveira ; João Alencar Pamphile ; Julio Cesar Polonio; Miriam Hiroko Inoue
This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.