Abstract
Entomopathogenic fungi interact with their insect hosts by infecting and colonizing their bodies as part of their life cycle. After breaching the host cuticle, a variety of toxic secondary metabolites is secreted into the hemocoel facilitating a successful invasion and colonization. The production of fungal toxins, e.g. beauvericin and destruxin in some model fungi such as Beauveria bassiana and Metarhizium anisopliae, represents a powerful defense tool system for the fungal species but also an opportunity to exploit its efficacy against prejudicial insects. Most of these compounds, such as non-ribosomal peptides, alkaloids, terpenes, and polyketides, are referred to as virulence factors and their synthesis and secretion regulation is tightly controlled. In the last decade few informations were available on how these metabolites work when secreted, and how to harness their potential regarding biological control applications. In recent years, with the advent of next-generation sequencing techniques and the advances in genetic manipulation of fungal species, vast information became available on the genes involved in the interaction between host and entomopathogenic fungi, including those involved in the synthesis and regulation of toxic secondary metabolite production. The design and application of transgenic entomopathogens with enhanced virulence factors are currently being addressed as a more effective alternative in traditional biological control strategies. The ecological importance of fungal secondary metabolites and virulence factors, and their role in the effectiveness of different species relying on toxins production, are key to enhance control of detrimental insect population, in an environmentally friendly and sustainable manner.
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References
Araujo, J. P. M., & Hughes, D. P. (2016). Diversity of entomopathogen fungi: Which groups conquered the insec body? Advances in Genetics, 94, 1–39.
Bilgo, E., Lovett, B., Fang, W., Bende, N., King, G. F., et al. (2017). Improved efficacy of an arthropod toxin expressing fungus against insecticide-resistant malaria-vector mosquitoes. Scientific Reports, 7, 3433.
Bilgo, E., Lovett, B., Bayili, K., Millogo, A. S., Saré, I., et al. (2018). Transgenic Metarhizium pingshaense synergistically ameliorates pyrethroid-resistance in wild-caught, malaria-vector mosquitoes. PLoS One, 13(9), e0203529.
Boucias, D., & Pendland, J. (1991). Attachment of mycopathogens to cuticle. The initial events of mycoses in arthropod hosts. In G. Cole & H. Hoch (Eds.), The fungal spore and disease initiation in plant and animals (pp. 101–127). Boston: Springer.
Boucias, D. G. & Pedland, J. C. (1998). Principles of insect pathology. Boston: Kluwer Academic Publishers.
Crespo, R., Juárez, M. P., Dal, B. G., Padín, S., Calderón, F. G., & Pedrini, N. (2002). Increased mortality of Acanthoscelides obtectus by alkane-grown Beauveria bassiana. BioControl, 47, 685–696.
Cross, A. (2008). What is a virulence factor? Critical Care, 12(6), 196.
de Bekker, C., Smith, P. B., Patterson, A. D., & Hughes, D. P. (2013). Metabolomics reveals the heterogeneous secretome of two entomopathogenic fungi to ex vivo cultured insect tissues. PLoS One, 8(8), e70609.
Eley, K. L., Halo, L. M., Song, Z., Powles, H., Cox, R. J., Bailey, A. M., et al. (2007). Biosynthesis of the 2-pyridone tenellin in the insect pathogenic fungus Beauveria bassiana. Chembiochem, 8, 289–297.
Fang, W., Leng, B., Xiao, Y., Jin, K., Fan, Y., et al. (2005). Cloning of Beauveria bassiana chitinase gene Bbchit1 and its application to improve fungal strain virulence. Applied and Enviromental Microbiology, 71, 363–370.
Fang, Y., Lou, M., Li, B., Xie, G.-L., Wang, F., et al. (2009). Characterization of Burkholderia cepacia complex from cystic fibrosis patients in China and their chitosan susceptibility. World Journal of Microbiology and Biotechnology, 26, 443–450.
Feng, P., Shang, Y., Cen, K., & Wang, C. (2015). Fungal biosynthesis of the bibenzoquinone oosporein to evade insect immunity. Proceedings of the National Academy of Sciences USA, 112, 11365–11370.
Ferron, P. (1985). Fungal control. In G. Kerkut & L. Gilbert (Eds.), Comprehensive insect physiology, biochemistry and pharmacology (pp. 313–346). New York: Academic Press.
Gao, Q., Jin, K., Ying, S., Zhang, Y., Xiao, G., et al. (2011). Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genetics, 7(1), e1001264.
Gibson, D. M., Donzelli, B. G., Krasnoff, S. B., & Keyhani, N. O. (2014). Discovering the secondary metabolite potential encoded within entomopathogenic fungi. Natural Product Reports, 31, 1287–1305.
Gonzalez, F., Tkaczuk, C., Dinu, M. M., Fiedler, Ż., Vidal, S., et al. (2016). New opportunities for the integration of microorganisms into biological pest control systems in greenhouse crops. Journal of Pest Science, 89, 295–311.
Hu, G., & St. Leger, R. J. (2002). Field studies using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent. Applied Environmental Microbiology, 68, 6383–6387.
Huarte-Bonnet, C., Juárez, M. P., & Pedrini, N. (2015). Oxidative stress in entomopathogenic fungi grown on insect-like hydrocarbons. Current Genetics, 61, 289–297.
Huarte-Bonnet, C., Kumar, S., Saparrat, M. C. N., Girotti, J. R., Santana, M., et al. (2018a). Insights into hydrocarbon assimilation by eurotialean and hypocrealean fungi: Roles for CYP52 and CYP53 clans of cytochrome P450 genes. Applied Biochemistry and Biotechnology, 184, 1047–1060.
Huarte-Bonnet, C., Paixão, F. R. S., Ponce, J. C., Santana, M., Prieto, E. D., & Pedrini, N. (2018b). Alkane-grown Beauveria bassiana produce mycelial pellets displaying peroxisome proliferation, oxidative stress, and cell surface alterations. Fungal Biology, 122, 457–464.
Joop, G., & Vilcinskas, A. (2016). Coevolution of parasitic fungi and insect hosts. Zoology, 119, 350–358.
Keyhani, N. O. (2018). Lipid biology in fungal stress and virulence: Entomopathogenic fungi. Fungal Biology, 122, 420–429.
Lobo, L. S., Luz, C., Fernandes, É. K. K., Juárez, M. P., & Pedrini, N. (2015). Assessing gene expression during pathogenesis: Use of qRT-PCR to follow toxin production in the entomopathogenic fungus Beauveria bassiana during infection and immune response of the insect host Triatoma infestans. Journal of Invertebrate Pathology, 128, 14–21.
Lovett, B., & St. Leger, R. J. (2017). The insect pathogens. Microbiology Spectrum, 5(2), FUNK-0001-2016. https://doi.org/10.1128/microbiolspec.FUNK-0001-2016.
Lovett, B., & St. Leger, R. J. (2018). Genetically engineering better fungal biopesticides. Pest Management Science, 74, 781–789.
Mannino, M. C., Juárez, M. P., & Pedrini, N. (2018). Tracing the coevolution between Triatoma infestans and its fungal pathogen Beauveria bassiana. Infection, Genetics and Evolution, 66, 319–324.
Mannino, M. C., Huarte-Bonnet, C., Davyt-Colo, B. & Pedrini, N. (2019). Is the insect cuticle the only entry gate for fungal infection? Insights into alternative modes of action of entomopathogenic fungi. Journal of Fungi, 5, 33. https://doi.org/10.3390/jof5020033.
Molnár, I., Gibson, D. M., & Krasnoff, S. B. (2010). Secondary metabolites from entomopathogenic Hypocrealean fungi. Natural Product Reports, 27, 1241.
Ortiz-Urquiza, A., & Keyhani, N. O. (2013). Action on the surface: Entomopathogenic fungi versus the insect cuticle. Insects, 4, 357–374.
Ortiz-Urquiza, A., & Keyhani, N. O. (2015). Molecular genetics of Beauveria bassiana infection of insects. Advances in Genetics, 94, 164–249.
Pedras, M. S. C., Zaharia, L. I., & Ward, D. E. (2002). The destruxins: Synthesis, biosynthesis, biotransformation, and biological activity. Phytochemistry, 59, 579–596.
Pedrini, N. (2018). Molecular interactions between entomopathogenic fungi (Hypocreales) and their insect host: Perspectives from stressful cuticle and hemolymph battlefields and the potential of dual RNA sequencing for future studies. Fungal Biology, 122, 538–545.
Pedrini, N., & Juárez, M. P. (2008). Entomopathogenic fungi and their host cuticle. In J. Capinera (Ed.), Encyclopedia of entomology (2nd ed., pp. 1333–1336). Heidelberg: Springer.
Pedrini, N., Juárez, M. P., Crespo, R., & de Alaniz, M. J. (2006). Clues on the role of Beauveria bassiana catalases in alkane degradation events. Mycologia. 98, 528-534. https://doi.org/10.1080/15572536.2006.11832655.
Pedrini, N., Crespo, R., & Juárez, M. P. (2007). Biochemistry of insect epicuticle degradation by entomopathogenic fungi. Comparative Biochemistry Physiology, 146(C), 124–137.
Pedrini, N., Mijailovsky, S. J., Girotti, J. R., Stariolo, R. M., & Cardozo R.Met al. (2009). Control of pyrethroid-resistant Chagas disease vectors with entomopathogenic fungi. PLoS Neglected Tropical Diseases, 3, e434.
Pedrini, N., Zhang, S., Juárez, M. P., & Keyhani, N. O. (2010). Molecular characterization and expression analysis of a suite of cytochrome P450 enzymes implicated in insect hydrocarbon degradation in the entomopathogenic fungus Beauveria bassiana. Microbiology, 156, 2549–2557.
Pedrini, N., Ortiz-Urquiza, A., Huarte-Bonnet, C., Zhang, S., & Keyhani, N. O. (2013). Targeting of insect epicuticular lipids by the entomopathogenic fungus Beauveria bassiana: Hydrocarbon oxidation within the context of a host-pathogen interaction. Frontiers in Microbiology, 4, 1–18.
Pedrini, N., Ortiz-Urquiza, A., Huarte-Bonnet, C., Fan, Y., Juárez, M. P., & Keyhani, N. O. (2015). Tenebrionid secretions and a fungal benzoquinone oxidoreductase form competing components of an arms race between a host and pathogen. Proceedings of the National Academy of Sciences USA, 112, E3651–E3660.
Pichersky, E., & Gang, D. R. (2000). Genetics and biochemistry of secondary metabolites in plants: An evolutionary perspective. Trends in Plant Science, 5, 439–445.
Qin, Y., Ying, S. H., Chen, Y., Shen, Z. C., & Feng, M. G. (2010). Integration of insecticidal protein Vip3aa1 into Beauveria bassiana enhances fungal virulence to Spodoptera litura larvae by cuticle and per os infection. Applied Environmental Microbiology, 76, 4611–4618.
Rohlfs, M., & Churchill, A. C. L. (2011). Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genetics and Biology, 48, 23–34.
St Leger, R. J., Joshi, L., Bidochka, M. J., & Roberts, D. W. (1996). Construction of an improved mycoinsecticide overexpressing a toxic protease. Proceedings of the National Academy of Sciences USA, 93, 6349–6354.
St. Leger, R. J., & Wang, C. (2010). Genetic engineering of fungal biocontrol agents to achieve greater efficacy against insect pests. Applied Microbiology and Biotechnology, 85, 901–907.
St. Leger, R. J., Bidochka, M. J., & Roberts, D. W. (1994). Isoforms of the cuticle-degrading Pr1 proteinase and production of a metalloproteinase by Metarhizium anisopliae. Archives of Biochemistry and Biophysics, 313, 1–7.
Süssmuth, R., Müller, J., Von Döhren, H., & Molnár, I. (2011). Fungal cyclooligomer depsipeptides: From classical biochemistry to combinatorial biosynthesis. Natural Products Reports, 28, 99–124.
Tobergte, D. R., & Curtis, S. (2013). Report from the commission to the european parliament and the council regarding trans fats in foods and in the overall diet of the union population. Journal of Chemical Information and Modeling, 53, 1689–1699.
Trienens, M., & Rohlfs, M. (2012). Insect-fungus interference competition – The potential role of global secondary metabolite regulation, pathway-specific mycotoxin expression and formation of oxylipins. Fungal Ecology, 5, 191–199.
Vilcinskas, A. (2010). Coevolution between pathogen-derived proteinases and proteinase inhibitors of host insects. Virulence, 1, 206–214.
Vilcinskas, A., & Götz, P. (1999). Parasitic fungi and their interactions with the insect immune system. Advances in Parasitology, 43, 267–313.
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 USA, 109, 1287–1292.
WHO. (2017). Vector-borne diseases [WWW Document]. URL https://www.who.int/news-room/fact-sheets/detail/vector-borne-diseases
Xiao, G., Ying, S. H., Zheng, P., Wang, Z. L., Zhang, S., et al. (2012). Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Scientific Reports, 2, 483.
Xu, Y., Orozco, R., Wijeratne, E. M. K., Gunatilaka, A. A. L., Stock, S. P., & Molnár, I. (2008). Biosynthesis of the cyclooligomer depsipeptide Beauvericin, a virulence factor of the entomopathogenic fungus Beauveria bassiana. Chemistry & Biology, 15, 898–907.
Xu, Y., Orozco, R., Kithsiri Wijeratne, E. M., Espinosa-Artiles, P., Gunatilaka, A. A. L., et al. (2009). Biosynthesis of the cyclooligomer depsipeptide bassianolide, an insecticidal virulence factor of Beauveria bassiana. Fungal Genetics and Biology, 46, 353–364.
Zhang, S., Widemann, E., Bernard, G., Lesot, A., Pinot, F., et al. (2012). CYP52X1, representing new cytochrome P450 subfamily, displays fatty acid hydroxylase activity and contributes to virulence and growth on insect cuticular substrates in entomopathogenic fungus Beauveria bassiana. Journal of Biological Chemistry, 287, 13477–13486.
Zhao, H., Lovett, B., & Fang, W. (2016). Genetically engineering entomopathogenic fungi. Advances in Genetics, 94, 137–163.
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Mannino, M.C., Davyt-Colo, B., Pedrini, N. (2021). Toxic Secondary Metabolites and Virulence Factors Expression by Entomopathogenic Fungi during Insect Infection and Potential Impact as a Tool for Pest Management. In: Khan, M.A., Ahmad, W. (eds) Microbes for Sustainable lnsect Pest Management. Sustainability in Plant and Crop Protection, vol 17. Springer, Cham. https://doi.org/10.1007/978-3-030-67231-7_6
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