Biopesticides: Mechanisms of biocidal action in pest insects

Authors

DOI:

https://doi.org/10.33448/rsd-v10i7.16893

Keywords:

Biological control; Entomopathogenic; Adhesin; Cry toxin.

Abstract

Insect pests are the main concern of farmers, this has led them to use inadequate control practices; causing an indiscriminated use of chemical pesticides which has resulted in the deterioration and disharmonization of the environment and human health. In recent years, biopesticides have been used as a healthy alternative for the control of pest insects whose biocidal action mechanisms motivated this review. In this article, 63 scientific research articles on entomopathogens were used from which 20 correspond to topics from a genetic approach (virulence genes), 23 articles detail the mechanisms of action by entomopathogenic fungi, 08 explain the mechanisms of action that exerts the bacterium Bacillus thuringiensis and 12 articles on characteristics of commercial microbial bioinsecticides. It can be concluded that fungi and bacteria are the most entomopathogenic microorganisms used in the formulation of biopesticides, being the species Metarhizium anisopliae, Beauveria bassiana and Bacillus thuringiensis the most used species. From this last, its biocidal effectiveness is based on the action of the Cry protein and of the first mentioned its effectiveness depends on the adhesion of the spore to the cuticle of the pest insect.

References

Altamira, P. (2020). Microorganismos con actividad entomopatogena. Boletin INIA-Instituto de Investigaciones Agropecuarias. https://biblioteca.inia.cl/handle/123456789/6899

Aw, K. M. S. & Hue, S. M. (2017). Mode of Infection of Metarhizium spp. Fungus and Their Potential as Biological Control Agents. Journal of Fungi, 3(2), 30. https://doi.org/10.3390/jof3020030

Baratto, C. M., Dutra, V., Boldo, J. T., Leiria, L. B., Vainstein, M. H. & Schrank, A. (2006). Isolation, Characterization, and Transcriptional Analysis of the Chitinase chi2 Gene (DQ011663) from the Biocontrol Fungus Metarhizium anisopliae var. Anisopliae. Current Microbiology, 53(3), 217-221. https://doi.org/10.1007/s00284-006-0078-6

Bilgo, E., Lovett, B., St. Leger, R. J., Sanon, A., Dabiré, R. K & Diabaté, A. (2018). Native entomopathogenic Metarhizium spp. From Burkina Faso and their virulence against the malaria vector Anopheles coluzzii and non-target insects. Parasites & Vectors, 11(1), 209. https://doi.org/10.1186/s13071-018-2796-6

Bravo, A., Gómez, I., Conde, J., Muñoz-Garay, C., Sánchez, J., Miranda, R., Zhuang, M., Gill, S. S. & Soberón, M. (2004). Oligomerization triggers binding of a Bacillus thuringiensis Cry1Ab pore-forming toxin to aminopeptidase N receptor leading to insertion into membrane microdomains. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1667(1), 38-46. https://doi.org/10.1016/j.bbamem.2004.08.013

Bravo, Pacheco, S., Gómez, I., Garcia-Gómez, B., Onofre, J. & Soberón, M. (2017). Insecticidal Proteins from Bacillus thuringiensis and Their Mechanism of Action. En L. M. Fiuza, R. A. Polanczyk y N. Crickmore (Eds.), Bacillus thuringiensis and Lysinibacillus sphaericus: Characterization and use in the field of biocontrol (pp. 53-66). Springer International Publishing. https://doi.org/10.1007/978-3-319-56678-8_4

Bustillo, A. (2001). Hongos e insectos y posibilidades de uso de control biológico de plagas en colombia. seminario Uso de entomopatógenos en Colombia. https://www.researchgate.net/publication/275462138_HONGOS_EN_INSECTOSy_POSIBILIDADES_DE_USO_EN_EL_CONTROL_BIOLOGICO_DE_PLAGAS_EN_COLOMBIA

Butt, T. M., Coates, C. J., Dubovskiy, I. M. & Ratcliffe, N. A. (2016). Chapter Nine - Entomopathogenic Fungi: New Insights into Host–Pathogen Interactions. En B. Lovett y R. J. St. Leger (Eds.), Advances in Genetics, 94, 307-364. https://doi.org/10.1016/bs.adgen.2016.01.006

Charnley, A. K. (1992). Mechanisms of fungal pathogenesis in insects with particular reference to locusts. https://agris.fao.org/agris-search/search.do?recordID=GB9124433

de Melo, N. R. de, Abdrahman, A., Greig, C., Mukherjee, K., Thornton, C., Ratcliffe, N. A., Vilcinskas, A. & Butt, T. M. (2013). Myriocin Significantly Increases the Mortality of a Non-Mammalian Model Host during Candida Pathogenesis. PLOS ONE, 8(11), e78905. https://doi.org/10.1371/journal.pone.0078905

Deng, C., Peng, Q., Song, F. & Lereclus, D. (2014). Regulation of cry Gene Expression in Bacillus thuringiensis. Toxins, 6(7), 2194-2209. https://doi.org/10.3390/toxins6072194

Donzelli, B. G. G., Krasnoff, S. B., Churchill, A. C. L., Vandenberg, J. D. & Gibson, D. M. (2010). Identification of a hybrid PKS–NRPS required for the biosynthesis of NG-391 in Metarhizium robertsii. Current Genetics, 56(2), 151-162. https://doi.org/10.1007/s00294-010-0288-0

Fang, W., Leng, B., Xiao, Y., Jin, K., Ma, J., Fan, Y., Feng, J., Yang, X., Zhang, Y. & Pei, Y. (2005). Cloning of Beauveria bassiana Chitinase Gene Bbchit1 and Its Application To Improve Fungal Strain Virulence. Applied and Environmental Microbiology, 71(1), 363-370. https://doi.org/10.1128/AEM.71.1.363-370.2005

Fang, W., Pei, Y. & Bidochka, M. (2007). A regulator of a G protein signalling (RGS) gene, cag8, from the insect-pathogenic fungus Metarhizium anisopliae is involved in conidiation, virulence and hydrophobin synthesis. Microbiology, 153, 1017-1025. https://doi.org/10.1099/mic.0.2006/002105-0

Fargues, J. (1984). Adhesion of the fungal spore to the insect cuticle in relation to pathogenicity. https://agris.fao.org/agris-search/search.do?recordID=US8719800

Feldhaar, H. & Gross, R. (2008). Immune reactions of insects on bacterial pathogens and mutualists. Microbes and Infection, 10(9), 1082-1088. https://doi.org/10.1016/j.micinf.2008.07.010

Fernández, C. & Juncosa, R. (2002). Biopesticidas:¿ la agricultura del futuro. Phytoma, 141, 14-19. https://infoxica2.files.wordpress.com/2010/01/1-12-biopesticidas-c2bf-la-agricultura-del-futuro.pdf

Freimoser, F. M., Grundschober, A., Tuor, U. & Aebi, M. (2003). Regulation of hyphal growth and sporulation of the insect pathogenic fungus Entomophthora thripidum in vitro. FEMS Microbiology Letters, 222(2), 281-287. https://doi.org/10.1016/S0378-1097(03)00315-X

Griko, N. B., Rose-Young, L., Zhang, X., Carpenter, L., Candas, M., Ibrahim, M. A., Junker, M. & Bulla, L. A. (2007). Univalent Binding of the Cry1Ab Toxin of Bacillus thuringiensis to a Conserved Structural Motif in the Cadherin Receptor BT-R1. Biochemistry, 46(35), 10001-10007. https://doi.org/10.1021/bi700769s

Güney, E., Adıgüzel, A., Demirbağ, Z. & Sezen, K. (2019). Bacillus thuringiensis kurstaki strains produce vegetative insecticidal proteins (Vip 3) with high potential. Egyptian Journal of Biological Pest Control, 29(1), 81. https://doi.org/10.1186/s41938-019-0180-2

Hajek, A. E. & St. Leger, R. J. (1994). Interactions Between Fungal Pathogens and Insect Hosts. Annual Review of Entomology, 39(1), 293-322. https://doi.org/10.1146/annurev.en.39.010194.001453

Hernandez-Fernandez, J. (2016). Bacillus thuringiensis: A natural tool in insect pest control. The handbook of microbial bioresources, 121-139. https://www.cabi.org/cabebooks/ebook/20163199951

Holder, D. J. & Keyhani, N. O. (2005). Adhesion of the Entomopathogenic Fungus Beauveria (Cordyceps) bassiana to Substrata. Applied and Environmental Microbiology, 71(9), 5260-5266. https://doi.org/10.1128/AEM.71.9.5260-5266.2005

Huang, W., Shang, Y., Chen, P., Gao, Q. & Wang, C. (2015). MrpacC regulates sporulation, insect cuticle penetration and immune evasion in Metarhizium robertsii. Environmental Microbiology, 17(4), 994-1008. https://doi.org/10.1111/1462-2920.12451

Ibarra, J. E. (2006). Los microorganismos en el control biológico de insectos y fitopatógenos. Rev Latinoam Microbiol, 8 https://www.medigraphic.com/pdfs/lamicro/mi-2006/mi062k.pdf

Jiang, H., Vilcinskas, A. & Kanost, M. R. (2010). Immunity in Lepidopteran Insects. En K. Söderhäll (Ed.), Invertebrate Immunity, 181-204. https://doi.org/10.1007/978-1-4419-8059-5_10

Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I., Frutos, R., Brownbridge, M. & Goettel, M. S. (2015). Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology, 132, 1-41. https://doi.org/10.1016/j.jip.2015.07.009

Lee, S. J., Lee, M. R., Kim, S., Kim, J. C., Park, S. E., Li, D., Shin, T. Y., Nai, Y.-S. & Kim, J. S. (2018). Genomic Analysis of the Insect-Killing Fungus Beauveria bassiana JEF-007 as a Biopesticide. Scientific Reports, 8(1), 12388. https://doi.org/10.1038/s41598-018-30856-1

Li, J., Ying, S.-H., Shan, L.-T. & Feng, M.-G. (2010). A new non-hydrophobic cell wall protein (CWP10) of Metarhizium anisopliae enhances conidial hydrophobicity when expressed in Beauveria bassiana. Applied Microbiology and Biotechnology, 85(4), 975-984. https://doi.org/10.1007/s00253-009-2083-8

Litwin, A., Nowak, M. & Różalska, S. (2020). Entomopathogenic fungi: Unconventional applications. Reviews in Environmental Science and Bio/Technology, 19(1), 23-42. https://doi.org/10.1007/s11157-020-09525-1

López-Pazos, S. A. & Cerón, J. (2010). Proteínas Cry de Bacillus thuringiensis y su interacción con coleópteros. NOVA, 8(14), Article 14. https://doi.org/10.22490/24629448.449

Moreno, I. M. A. (2012). Bacillus thuringiensis, el ingrediente activo de bioinsecticidas. 17(63). http://www.comprendamos.org/alephzero/63/aleph63.pdf

Muñoz T., P. A. (2018). Microorganismos como una alternativa al uso de agroquímicos. Idesia (Arica), 36(1), 3-5. https://doi.org/10.4067/S0718-34292018000100003

Ortiz-Urquiza, A. & Keyhani, N. O. (2013). Action on the surface: Entomopathogenic fungi versus the insect cuticle. Insects 4: 357–374. https://pubmed.ncbi.nlm.nih.gov/26462424/

Pedrini, N., Crespo, R. & Juárez, M. P. (2007). Biochemistry of insect epicuticle degradation by entomopathogenic fungi. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 146(1), 124-137. https://doi.org/10.1016/j.cbpc.2006.08.003

Pigott, C. R. & Ellar, D. J. (2007). Role of Receptors in Bacillus thuringiensis Crystal Toxin Activity. Microbiology and Molecular Biology Reviews, 71(2), 255-281. https://doi.org/10.1128/MMBR.00034-06

Pucheta, M., Flores-Macías, A., Rodríguez-Navarro, S. y Torre, M. (2006). Mecanismo de acción de los hongos entomopatógenos. Interciencia: Revista de ciencia y tecnología de América, 31(12), 856-860. https://www.redalyc.org/pdf/339/33901204.pdf

Roberts, D. W. & Humber, R. A. (1981). Entomogenous fungi. Biology of conidial fungi, 2(201), e236. https://www.scirp.org/(S(351jmbntvnsjt1aadkposzje))/reference/ReferencesPapers.aspx?ReferenceID=1535851

Rother, E. T. (2007). Revisão sistemática x Revisão Narrativa. Acta Paulista de Enfermagem, 20(2).

Rosas-García, N. M., Avalos-de-León, O., Villegas-Mendoza, J. M., Mireles-Martínez, M., Barboza-Corona, J. E. & Castañeda-Ramírez, J. C. (2014). Correlation between Pr1 and Pr2 gene content and virulence in Metarhizium anisopliae strains. Journal of Microbiology and Biotechnology, 24(11), 1495-1502. https://doi.org/10.4014/jmb.1404.04044

Samuels, R., Paula, A., Carolino, A., Gomes, S., Paula, C., Cypriano, M., Silva, L., Ribeiro, A., Bastos, J. & Peres, C. (2016). Entomopathogenic organisms: Conceptual advances and real-world applications for mosquito biological control. Open Access Insect Physiology, 25. https://doi.org/10.2147/OAIP.S68850

Sanchis, V. y Bourguet, D. (2009). Bacillus thuringiensis: Applications in Agriculture and Insect Resistance Management - A Review. En E. Lichtfouse, M. Navarrete, P. Debaeke, S. Véronique y C. Alberola (Eds.), Sustainable Agriculture, 243-255. https://doi.org/10.1007/978-90-481-2666-8_16

Santi, L., Beys da Silva, W. O., Berger, M., Guimarães, J. A., Schrank, A. & Vainstein, M. H. (2010). Conidial surface proteins of Metarhizium anisopliae: Source of activities related with toxic effects, host penetration and pathogenesis. Toxicon, 55(4), 874-880. https://doi.org/10.1016/j.toxicon.2009.12.012

Schnepf, E., Crickmore, N., Rie, J. V., Lereclus, D., Baum, J., Feitelson, J., Zeigler, D. R. & Dean, D. H. (1998). Bacillus thuringiensis and Its Pesticidal Crystal Proteins. Microbiology and Molecular Biology Reviews, 62(3), 775-806. https://doi.org/10.1128/MMBR.62.3.775-806.1998

SENASA (2021). Lista de productos biologicos formulados registrados. https://www.senasa.gob.pe/senasa/insumos-inocuidad-organica-semillas/

Sevim, A., Donzelli, B., Wu, D., Demirbag, Z., Gibson, D. & Turgeon, G. (2012). Hydrophobin genes of the entomopathogenic fungus, Metarhizium brunneum, are diVerentially expressed and corresponding mutants are decreased in virulence. Current genetics, 58, 79-92. https://doi.org/10.1007/s00294-012-0366-6

Shang, Y., Chen, P., Chen, Y., Lu, Y. & Wang, C. (2015). MrSkn7 Controls Sporulation, Cell Wall Integrity, Autolysis, and Virulence in Metarhizium robertsii. Eukaryotic Cell, 14(4), 396-405. https://doi.org/10.1128/EC.00266-14

Sharma, A., Srivastava, A., Shukla, A. K., Srivastava, K., Srivastava, A. K. & Saxena, A. K. (2020). Entomopathogenic Fungi: A Potential Source for Biological Control of Insect Pests. En M. K. Solanki, P. L. Kashyap y B. Kumari (Eds.), Phytobiomes: Current Insights and Future Vistas, 225-250. https://doi.org/10.1007/978-981-15-3151-4_9

Skinner, M., Parker, B. L. & Kim, J. S. (2014). Chapter 10—Role of Entomopathogenic Fungi in Integrated Pest Management. En D. P. Abrol (Ed.), Integrated Pest Management, 169-191. https://doi.org/10.1016/B978-0-12-398529-3.00011-7

Tanada, Y. & Kaya, H. K. (2012). Insect Pathology. Academic Press. https://www.sciencedirect.com/book/9780123849847/insect-pathology

Téllez-Jurado, A., Cruz Ramírez, M. G., Mercado Flores, Y., Asaff Torres, A. & Arana-Cuenca, A. (2009). Mecanismos de acción y respuesta en la relación de hongos entomopatógenos e insectos. Revista mexicana de micología, 30, 73-80. https://www.researchgate.net/publication/237041725_Mecanismos_de_accion_y_respuesta_en_la_relacion_de_hongos_entomopatogenos_e_insectos

Uchida, R., Imasato, R., Yamaguchi, Y., Masuma, R., Shiomi, K., Tomoda, H. & Ōmura, S. (2005). New Insecticidal Antibiotics, Hydroxyfungerins A and B, Produced by Metarhizium sp. FKI-1079. The Journal of Antibiotics, 58(12), 804-809. https://doi.org/10.1038/ja.2005.107

Vachon, V., Laprade, R. & Schwartz, J.-L. (2012). Current models of the mode of action of Bacillus thuringiensis insecticidal crystal proteins: A critical review. Journal of Invertebrate Pathology, 111(1), 1-12. https://doi.org/10.1016/j.jip.2012.05.001

Villarreal-Delgado, M. F., Villa-Rodríguez, E. D., Cira-Chávez, L. A., Estrada-Alvarado, M. I., Parra-Cota, F. I., Santos-Villalobos, S. de los, Villarreal-Delgado, M. F., Villa-Rodríguez, E. D., Cira-Chávez, L. A., Estrada-Alvarado, M. I., Parra-Cota, F. I. & Santos-Villalobos, S. de los. (2018). El género Bacillus como agente de control biológico y sus implicaciones en la bioseguridad agrícola. Revista mexicana de fitopatología, 36(1), 95-130. https://doi.org/10.18781/r.mex.fit.1706-5

Wang, B., Kang, Q., Lu, Y., Bai, L. & Wang, C. (2012). Unveiling the biosynthetic puzzle of destruxins in Metarhizium species. Proceedings of the National Academy of Sciences, 109(4), 1287-1292. https://doi.org/10.1073/pnas.1115983109

Wang, C. & Leger, R. J. S. (2006). A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proceedings of the National Academy of Sciences, 103(17), 6647-6652. https://doi.org/10.1073/pnas.0601951103

Wang, C., Typas, M. A. & Butt, T. M. (2002). Detection and characterisation of pr1 virulent gene deficiencies in the insect pathogenic fungus Metarhizium anisopliae. FEMS Microbiology Letters, 213(2), 251-255. https://doi.org/10.1111/j.1574-6968.2002.tb11314.x

Wang, J., Chen, J., Hu, Y., Ying, S.-H. & Feng, M.-G. (2020). Roles of six Hsp70 genes in virulence, cell wall integrity, antioxidant activity and multiple stress tolerance of Beauveria bassiana. Fungal Genetics and Biology, 144, 103437. https://doi.org/10.1016/j.fgb.2020.103437

Xie, T., Wang, Y., Yu, D., Zhang, Q., Zhang, T., Wang, Z. & Huang, B. (2019). MrSVP, a secreted virulence-associated protein, contributes to thermotolerance and virulence of the entomopathogenic fungus Metarhizium robertsii. BMC Microbiology, 19(1), 25. https://doi.org/10.1186/s12866-019-1396-8

Xu, C., Wang, B.-C., Yu, Z. & Sun, M. (2014). Structural Insights into Bacillus thuringiensis Cry, Cyt and Parasporin Toxins. Toxins, 6(9), 2732-2770. https://doi.org/10.3390/toxins6092732

Zhang, Y., Zhao, J., Fang, W., Zhang, J., Luo, Z., Zhang, M., Fan, Y. & Pei, Y. (2009). Mitogen-activated protein kinase hog1 in the entomopathogenic fungus Beauveria bassiana regulates environmental stress responses and virulence to insects. Applied and Environmental Microbiology, 75(11), 3787-3795. https://doi.org/10.1128/AEM.01913-08

Zhou, G., Ying, S.-H., Hu, Y., Fang, X., Feng, M.-G. & Wang, J. (2018). Roles of Three HSF Domain-Containing Proteins in Mediating Heat-Shock Protein Genes and Sustaining Asexual Cycle, Stress Tolerance, and Virulence in Beauveria bassiana. Frontiers in Microbiology, 9. https://doi.org/10.3389/fmicb.2018.01677

Zhu, Y., Pan, J., Qiu, J. & Guan, X. (2008). Isolation and characterization of a chitinase gene from entomopathogenic fungus Verticillium lecanii. Brazilian Journal of Microbiology, 39(2), 314-320. https://doi.org/10.1590/S1517-83822008000200022

Downloads

Published

27/06/2021

How to Cite

MIRANDA , A. V. C. .; ESPEJO, Y. del C. B.; SALAS , J. L. T. F. .; GONZALES , H. H. S. .; AGUILERA, J. G. .; MARTÍNEZ, L. A. . Biopesticides: Mechanisms of biocidal action in pest insects. Research, Society and Development, [S. l.], v. 10, n. 7, p. e42010716893, 2021. DOI: 10.33448/rsd-v10i7.16893. Disponível em: https://www.rsdjournal.org/index.php/rsd/article/view/16893. Acesso em: 16 apr. 2024.

Issue

Vol. 10 No. 7

Section

Agrarian and Biological Sciences

License

Copyright (c) 2021 Angela Verónica Choque Miranda ; Yemile del Carmen Berrios Espejo; Jorge Luis Tomas Florez Salas ; Hebert Hernan Soto Gonzales ; Jorge González Aguilera; Leandris Argentel Martínez

Creative Commons License

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.