Abstract
Research and commercial production of bioherbicides occur to a lesser extent compared to bioinsecticides and biofungicides. In order to contribute to developing new bioherbicides with low environmental impact, this study aimed to increase the phytotoxicity of metabolites of the fungus Mycoleptodiscus indicus UFSM 54 by optimizing solid and submerged fermentation and evaluate the ecotoxicological effects on earthworms (Eisenia andrei). The Plackett–Burman and central composite rotatable designs were used to optimize metabolite phytotoxicity. The variables optimized in the fermentation were temperature, agitation, pH, water volume in the culture medium, glucose concentration, and yeast extract. The fungus was grown on sugarcane bagasse substrate, and its metabolites were applied to detached Cucumis sativus, Conyza sp., and Sorghum bicolor leaves and used in an avoidance test and acute exposure to earthworms. Metabolite phytotoxicity in submerged fermentation was optimized at 35 °C, 50 rpm, and 1.5 g l−1 of glucose and in solid fermentation at 30–37 °C and in 14–32 ml of water. The metabolites severely damaged germination, initial growth, and leaves of the three plants, and at the doses tested (maximum of 113.92 ml kg−1), the metabolites of M. indicus UFSM 54 were not toxic to earthworms.
Similar content being viewed by others
Availability of data and material
Availability of data and materials: The strain Mycoleptodiscus indicus UFSM 54 was preserved in Laboratory of Soil Biology at the Federal University of Santa Maria, Brazil.
Code availability
Not applicable.
References
Andrighetti, M. S., Nachtigall, G. R., Nascimento de Queiroz, S. C., Ferracini, V. L., & Ayub, M. A. Z. (2014). Biodegradation of glyphosate by microbiota of soils of apple tree fields. Rev. Bras. Cienc. Solo, 38, 1643–1653. https://doi.org/10.1590/S0100-06832014000500029
Leoci, R., Ruberti, M. (2020) Glyphosate in Agriculture: Environmental Persistence and Effects on Animals. J Agric. Environ. Int. Dev. 114:99–122. https://doi.org/10.12895/jaeid.20201.1167
Maggi, F., Cecilia, D., Tang, F. H. M., & McBratney, A. (2020). The global environmental hazard of glyphosate use. Science of the Total Environment, 717, 137167. https://doi.org/10.1016/j.scitotenv.2020.137167
Vera, M. S., Fiori, E. D., Lagomarsino, L., Sinistro, R., Escaray, R., Iummato, M. M., Juárez, A., Molina, M. C. R., Tell, G., & Pizarro, H. (2012). Direct and indirect effects of the glyphosate formulation Glifosato Atanor® on freshwater microbial communities. Ecotoxicology, 21, 1805–1816. https://doi.org/10.1007/s10646-012-0915-2
Santos, F. M., Vargas, L., Christoffoleti, P. J., Agostinetto, D., Mariani, F., & Dal Magro, T. (2014). Differential susceptibility of biotypes of Conyza sumatrensis to chlorimuron-ethyl herbicide. Planta Daninha, 32, 427–435. https://doi.org/10.1590/S0100-83582014000200021
Radhakrishnan, R., Alqarawi, A. A., & Abd Allah, E. F. (2018). Bioherbicides: Current knowledge on weed control mechanism. Ecotox. Environ. Safe, 158, 131–138. https://doi.org/10.1016/j.ecoenv.2018.04.018
Keswani, C., Singh, H. B., Hermosa, R., García-Estrada, C., Caradus, J., He, Y. W., Mezaache-Aichour, S., Glare, T. R., Borriss, R., Vinale, F., & Sansinenea, E. (2019). Antimicrobial secondary metabolites from agriculturally important fungi as next biocontrol agents. Appl. Microbiol. Biot., 103, 9287–9303. https://doi.org/10.1007/s00253-019-10209-2
Varejão, E. V. V., Demuner, A. J., Barbosa, L. C. A., Barreto, R. W., & Vieira, B. (2013). Toxidade de Filtrados de Cultura de Alternaria euphorbiicola em folhas de Euphorbia heterophylla. Planta Daninha, 31, 1–9. https://doi.org/10.1590/S0100-83582013000100001
Romdhane, S., Devers-Lamrani, M., Barthelmebs, L., Calvayrac, C., Bertrand, C., Cooper, J. F., Dayan, F. E., & Laurent, F. M. (2016). Ecotoxicological impact of the bioherbicide leptospermone on the microbial community of two arable soils. Frontiers in Microbiology, 7, 1–12. https://doi.org/10.3389/fmicb.2016.00775
MAPA. Ministério da Agricultura, Pecuária e Abastecimento. (2021) AGROFIT, Brazil. https://www.gov.br/agricultura/pt-br/assuntos/insumos-agropecuarios/insumos-agricolas/agrotoxicos/agrofit. Accessed 10August 2021
Qiu, P., Feng, Z. X., Tian, J. W., Lei, Z. C., Wang, L., Zeng, Z. G., Chu, Y. W., & Tian, Y. Q. (2015). Diversity, bioactivities, and metabolic potentials of endophytic actinomycetes isolated from traditional medicinal plants in Sichuan, China Chinese. Journal of Natural Medicines, 13, 942–953. https://doi.org/10.1016/S1875-5364(15)30102-3
Perotti, V. E., Larran, A. S., Palmieri, V. E., Martinatto, A. K., & Permingeat, H. R. (2020). Herbicide resistant weeds: A call to integrate conventional agricultural practices, molecular biology knowledge and new technologies. Plant Science, 290, 110255. https://doi.org/10.1016/j.plantsci.2019.110255
Bonny, S. (2017). Genetically Modified Herbicide-Tolerant Crops, Weeds, and Herbicides: Overview and Impact. Biological Control, 10, 1–9. https://doi.org/10.1007/s00267-015-0589-7
Fumagalli, P., Andolfi, A., Avolio, F., Boari, A., Cimmino, A., & Finizio, A. (2012). Ecotoxicological characterisation of a mycoherbicide mixture isolated from the fungus Ascochyta caulina. Pest Management Science, 69, 850–856. https://doi.org/10.1002/ps.3447
Portela, V. O., Moro, A., Santana, N. A., Baldoni, D. B., Castro, I. A., Antoniolli, Z. I., Dalcol, I. I., & Jacques, R. J. S. (2020). First report on the production of phytotoxic metabolites by Mycoleptodiscus indicus under optimized conditions of submerged fermentation. Environmental Technology. https://doi.org/10.1080/09593330.2020.1836030
Souza, A. R. C., Baldoni, D. B., Lima, J., Porto, V., Marcuz, C., Machado, C., Ferraz, R. C., Kuhn, R. C., Jacques, R. J. S., Guedes, J. V. C., & Mazutti, M. A. (2017). Selection, isolation, and identification of fungi for bioherbicide production. Brazilian Journal of Microbiology, 48, 101–108. https://doi.org/10.1016/j.bjm.2016.09.004
Frans, R., Crowler, H. (1986). In: Camper ND (ed) Research Methods in Weed Science. Southern Weed Science Society, 3rd edn. Champaign.
Brasil. (2009). Regras Para Análise de Sementes. Teste de Germinação. Ministério da Agricultura, Pecuária e Abastecimento (MAPA), Brasília.
Vidal, R. A., Kalsing, A., Goulart, I. C. G. R., Lamego, F. P., & Christoffoleti, P. J. (2007). Impacto da temperatura, irradiância e profundidade das sementes na emergência e germinação de Conyza bonariensis e Conyza canadensis resistentes ao glyphosate. Planta Daninha, 25, 309–315. https://doi.org/10.1590/S0100-83582007000200010
Nakagawa, J. (1999) In: Krzyzanoski, F.C., Vieira, R.D., França Neto, J.B. (ed) Vigor de sementes: conceitos e testes (1 st). ABRATES, Londrina.
Mendes, I. S., & Rezende, M. O. O. (2014). Assessment of the allelopathic effect of leaf and seed extracts of Canavalia ensiformis as post emergent bioherbicides: A green alternative for sustainable agriculture. J. Environ. Sci. Health B: Pesticides, Food Contaminants, and Agricultural Wastes, 49, 374–380. https://doi.org/10.1080/03601234.2014.882179
Radwan, M. A., Farrag, S. A. A., Abu-Elamayem, M. M., & Ahmed, N. S. (2012). Biological control of the root-knot nematode, Meloidogyne incognita on tomato using bioproducts of microbial origin. Applied Soil Ecology, 56, 58–62. https://doi.org/10.1016/j.apsoil.2012.02.008
ABNT. Brazilian Association of Technical Standards NBR ISO 17512–1 (2011) Soil quality: leakage test to assess soil quality and effects of chemical substances on behavior: Part 1: earthworm test (Eisenia fetida and Eisenia andrei). Rio de Janeiro.
OECD. Organization for Economic Co-operation and Development (2004) Guideline for the testing of chemicals. Earthworm Reproduction Test (Eisenia fetida/ Eisenia andrei)
Ferreira, D. F. (2014). Sisvar: A Guide for its Bootstrap procedures in multiple comparisons. Cienc. Agrotec., 38, 109–112. https://doi.org/10.1590/S1413-70542014000200001
ABNT. Brazilian Association of Technical Standards NBR 15537 (2007) Terrestrial ecotoxicology – Acute ecotoxicity – Earthworm test method. Rio de Janeiro.
Andrioli, W. J., Conti, R., Araújo, M. J., Zanasi, R., Cavalcanti, B. C., Manfrim, V., Toledo, J. S., Tedesco, D., Moraes, M. O., Pessoa, C., Cruz, A. K., Bertucci, C., Sabino, J., Nanayakkara, D. N. P., Pupo, M. T., & Bastos, J. K. (2014). Mycoleptones A-C and polyketides from the endophyte Mycoleptodiscus indicus. Journal of Natural Products, 77, 70–78. https://doi.org/10.1021/np4006822
Ahmed, T., Pattnaik, S., Khan, M. B., Ampasala, D. R., Busi, S., & Sarma, V. V. (2020). Inhibition of quorum sensing–associated virulence factors and biofilm formation in Pseudomonas aeruginosa PAO1 by Mycoleptodiscus indicus PUTY1. Brazilian Journal of Microbiology, 51, 467–487. https://doi.org/10.1007/s42770-020-00235-y
Pandey, A. (2003). Solid state fermentation. Biochemical Engineering Journal, 13, 81–84. https://doi.org/10.1016/S1369-703X(02)00121-3
El-Feky, R.M., Abdel Fattah, A.A., Gibriel, A.Y., Farag, A.A. (2019) Optimization the Parameter Process of Solid-State Fermentation to Produce the Fungal α-amylase on Agro-Industrial By-Products. Arab Universities Journal of Agricultural Sciences 27:441–454. https://doi.org/10.21608/AJS.2019.43583
Khanahmadi, M., Arezi, I., Amiri, M. S., & Miranzadeh, M. (2018). Bioprocessing of agro-industrial residues for optimization of xylanase production by solid- state fermentation in flask and tray bioreactor. Biocatalysis and Agricultural Biotechnology, 13, 272–282. https://doi.org/10.1016/j.bcab.2018.01.005
Webb, C., Manan, M.A. (2017) Design aspects of solid state fermentation as applied to microbial bioprocessing. J. Appl. Biotechnol. Bioeng. 4:511–532. https://doi.org/10.15406/jabb.2017.04.00094
Lonsane, B. K., & Ramesh, M. V. (1990). Production of bacterial thermostable α-amylase by solid-state fermentation: A potential tool for achieving economy in enzyme production and starch hydrolysis. Advances in Applied Microbiology, 35, 1–56. https://doi.org/10.1016/S0065-2164(08)70242-9
Sodhi, H. K., Sharma, K., Gupta, J. K., & Soni, S. K. (2005). Production of a thermostable α -amylase from Bacillus sp. PS-7 by solid state fermentation and its synergistic use in the hydrolysis of malt starch for alcohol production. Process Biochemistry, 40, 525–534. https://doi.org/10.1016/j.procbio.2003.10.008
Gonçalves, F. A., Leite, R. S. R., Rodrigues, A., Argandoña, E. J. S., & Fonseca, G. G. (2013). Isolation, identification and characterization of a novel high level β-glucosidase producing Lichtheimia ramosa strain. Biocatalysis and Agricultural Biotechnology, 16, 377–384. https://doi.org/10.1016/j.bcab.2013.06.006
Matkar, K., Chapla, D., Divecha, J., Nighojkar, A., & Madamwar, D. (2013). Production of cellulase by a newly isolated strain of Aspergillus sydowii and its optimization under submerged fermentation. International Biodeterioration & Biodegradation, 78, 24–33. https://doi.org/10.1016/j.ibiod.2012.12.002
Souza, A. R. C., Baldoni, D. B., Lima, J., Porto, V., Marcuz, C., Ferraz, R. C., Kuhn, R. C., Jacques, R. J. S., Guedes, J. V. C., & Mazutti, M. A. (2015). Bioherbicide production by Diaporthe sp. isolated from the Brazilian Pampa biome. Biocatalysis and Agricultural Biotechnology, 4, 575–578. https://doi.org/10.1016/j.bcab.2015.09.005
Brun, T., Rabuske, J.E., Todero, I., Almeida, T.C., Junior, J.J.D., Ariotti, G., Confortin, T., Arnemann, J.A., Kuhn, R.C., Guedes, J.V.C., Mazutti, M.A. (2016) Production of bioherbicide by Phoma sp. in a stirred-tank bioreactor. 3 Biotech 6:230–237. https://doi.org/10.1007/s13205-016-0557-9
Brun, T., Rabuske, J. E., Confortin, T. C., Luft, L., Todero, I., Fischer, M., Zabot, G. L., & Mazutti, M. A. (2022). Weed control by metabolites produced from Diaporthe schini. Environmental Technology, 43, 139–148. https://doi.org/10.1080/09593330.2020.1780477
Kobakhidze, A., Asatiani, M., Kachlishvili, E., & Elisashvili, V. (2016). Induction and catabolite repression of cellulase and xylanase synthesis in the selected white-rot basidiomycetes. Ann. Agrar. Sci., 14, 169–176. https://doi.org/10.1016/j.aasci.2016.07.001
Liu, J., Yang, J., Wang, R., Liu, L., Zhang, Y., Bao, H., Jang, J. M., Wang, E., & Yuan, H. (2020). Comparative characterization of extracellular enzymes secreted by Phanerochaete chrysosporium during solid-state and submerged fermentation. International Journal of Biological Macromolecules, 152, 288–294. https://doi.org/10.1016/j.ijbiomac.2020.02.256
Sepúlveda, L., Laredo-Alcalá, E., Buenrostro-Figueroa, J. J., Ascacio-Valdés, J. A., Genisheva, Z., Aguilar, C., & Teixeira, J. (2020). Ellagic acid production using polyphenols from orange peel waste by submerged fermentation Electronic. Journal of Biotechnology, 43, 1–7. https://doi.org/10.1016/j.ejbt.2019.11.002
Wei, Y. Y., Chou, K. C. C., Yang, S. H., & Chiang, B. H. (2020). Oxygen vector accelerates farnesylation and redoxreaction to promote the biosynthesis of4-acetylantroquinonol B and antroquinonol during submerged fermentation of Antrodia cinnamomea. Food and Bioproducts Processing, 20, 80–90. https://doi.org/10.1016/j.fbp.2019.12.012
Agboyibor, C., Kong, W.B., Zhang, A.M., Niu, S.Q. (2019) Nutrition regulation for the production of Monascus red and yellow pigment with submerged fermentation by Monascus purpureus. Biocatal. Agric. Biotechnol. 21: 101276.
El-Gholl, N. E., & Alfieri, S. A. (1991). Leaf necrosis of Zamia caused by Mycoleptodiscus indicus. Plant. Pathol. Circular, 349, 1–2.
Bailey, K. L., Pitt, W. M., Falk, S., & Derby, J. (2011). The effects of Phoma macrostoma on nontarget plant and target weed species. Biological Control, 58, 379–386. https://doi.org/10.1016/j.biocontrol.2011.06.001
Sales Junior, S. F., Vallerie, Q., Araujo, G. F., Soares, L. O. S., Silva, E. O., Correia, F. V., & Saggioro, E. M. (2020). Triclocarban affects earthworms during long-term exposure: Behavior, cytotoxicity, oxidative stress and genotoxicity assessments. Environmental Pollution, 267, 115570. https://doi.org/10.1016/j.envpol.2020.115570
Clasen, B., Lisbôa, R.M. (2019) In: Vázquez-Luna, D., Cuevas-Díaz, M.deC. (ed) Soil Contamination and Alternatives for Sustainable Development. IntechOpen, Rijeka, Croatia.
Soares, K.W.P., Mariano, W.S., Paulino, M.G. (2020) Avoidance test with earthworms (Eisenia andrei) in natural soil treated with a Bacillus thuringiensis based biopesticide to soil quality evaluation. Res. Soc. Dev. 9:e423985774. https://doi.org/10.33448/rsd-v9i8.5774
Shao, H., & Zhang, Y. (2017). Non-target effects on soil microbial parameters of the synthetic pesticide carbendazim with the biopesticides cantharidin and norcantharidin. Science and Reports, 7, 1–12. https://doi.org/10.1038/s41598-017-05923-8
Pino-Otín, M. R., Val, J., Ballestero, D., Navarro, E., Sánchez, E., González-Coloma, A., & Mainar, A. M. (2019). Ecotoxicity of a new biopesticide produced by Lavandula luisieri on non-target soil organisms from different trophic levels. Science of the Total Environment, 671, 83–93. https://doi.org/10.1016/j.scitotenv.2019.03.293
Schnug, L., Jensen, J., Scott-Fordsmand, J. J., & Leinaas, H. P. (2014). Toxicity of three biocides to springtails and earthworms in a soil multi-species (SMS) test system. Soil Biology & Biochemistry, 74, 115–126. https://doi.org/10.1016/j.soilbio.2014.03.007
Marques, N. P., Pereira, J. C., Gomes, E., Silva, R., Araújo, A. R., Ferreira, H., Rodrigues, A., Dussána, K. J., & Bocchini, D. A. (2018). Cellulases and xylanases production by endophytic fungi by solid state fermentation using lignocellulosic substrates and enzymatic saccharification of pretreated sugarcane bagasse. Industrial Crops and Products, 122, 66–75. https://doi.org/10.1016/j.indcrop.2018.05.022
Salomao, G. S. B., Agnezi, J. C., Paulino, L. B., Hencker, L. B., Shimosakai, T. L., Tardioli, P. W., & Pinotti, L. M. (2019). Production of cellulases by solid state fermentation using natural and pretreated sugarcane bagasse with different fungi. Biocatalysis and Agricultural Biotechnology, 17, 1–6. https://doi.org/10.1016/j.bcab.2018.10.019
Attias, N., Danai, O., Abitbol, T., Tarazi, E., Ezov, N., Pereman, I., & Grobman, Y. J. (2020). Mycelium bio-composites in industrial design and architecture: Comparative review and experimental analysis. Journal of Cleaner Production, 246, 19037. https://doi.org/10.1016/j.jclepro.2019.119037
Membrillo, I., Sánchez, C., Meneses, M., Favela, E., & Loera, O. (2008). Effect of substrate particle size and additional nitrogen source on production of lignocellulolytic enzymes by Pleurotus ostreatus strains. Bioresource Technol., 99, 7842–7847. https://doi.org/10.1016/j.biortech.2008.01.083
Ottati-de-Lima, E. L., Batista Filho, A., Almeida, J. E. M., Gassen, M. H., Wenzel, I. M., Almeida, A. M. B., & Zapellini, L. O. (2014). Liquid production of entomopathogenic fungi and ultraviolet radiation and temperature effects on produced propagules. Arquivos do Instituto Biológico, 81, 342–350. https://doi.org/10.1590/1808-1657001352012
Shabana, Y. M., Charudattan, R., Abou Tabl, A. H., Morales-Payan, J. P., Rosskopf, E. N., & Klassen, W. (2010). Production and application of the bioherbicide agent Dactylaria higginsii on organic solid substrates. Biological Control, 54, 159–165. https://doi.org/10.1016/j.biocontrol.2010.05.002
Acknowledgements
The authors thank the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq); the Brazilian Federal Agency for the Support and Evaluation of Graduate Education (Coordenação de Aperfeiçoamento Pessoal de Nível Superior, CAPES), Finance Code 001; for scholarships and funding support. We also thank the members of the Laboratory of Soil Biology at the Federal University of Santa Maria for their involvement in this study.
Funding
This study was supported by the National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq); the Brazilian Federal Agency for the Support and Evaluation of Graduate Education (Coordenação de Aperfeiçoamento Pessoal de Nível Superior, CAPES), Finance Code 001.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflicts of interest/Competing interests
The authors declare that there are no conflicts of interest associated with the work presented.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Portela, V.O., Santana, N.A., Balbinot, M.L. et al. Phytotoxicity Optimization of Fungal Metabolites Produced by Solid and Submerged Fermentation and its Ecotoxicological Effects. Appl Biochem Biotechnol 194, 2980–3000 (2022). https://doi.org/10.1007/s12010-022-03884-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12010-022-03884-x