Three-dimensional cellular aggregates formed by Beauveria pseudobassiana in liquid culture with potential for use as a biocontrol agent of the African black beetle (Heteronychus arator)

References

• Allocati N, Masulli M, Di Ilio C, De Laurenzi V. 2015. Die for the community: an overview of programmed cell death in bacteria. Cell Death Dis. 6:e1609. doi:https://doi.org/10.1038/cddis.2014.570.
   PubMed Web of Science ®Google Scholar
• Beauvais A, Loussert C, Prevost MC, Verstrepen K, Latgé JP. 2009. Characterization of a biofilm‐like extracellular matrix in FLO1‐expressing Saccharomyces cerevisiae cells. FEMS Yeast Res. 9:411–419. doi:https://doi.org/10.1111/j.1567-1364.2009.00482.x.
   PubMedGoogle Scholar
• Boucias DG, Pendland JC, Latge JP. 1988. Nonspecific factors involved in attachment of entomopathogenic deuteromycetes to host insect cuticle. Appl Environ Microbiol. 54:1795–1805. doi:https://doi.org/10.1128/AEM.54.7.1795-1805.1988.
   PubMed Web of Science ®Google Scholar
• Cavalheiro M, Teixeira MC. 2018. Candida biofilms: threats, challenges, and promising strategies. Front Med. 5:28. doi:https://doi.org/10.3389/fmed.2018.00028.
   PubMed Web of Science ®Google Scholar
• Chaffin WL. 2008. Candida albicans cell wall proteins. Microbiol Mol Biol Rev. 72:495–544. doi:https://doi.org/10.1128/MMBR.00032-07.
   PubMed Web of Science ®Google Scholar
• Cho EM, Liu L, Farmerie W, Keyhani NO. 2006. EST analysis of cDNA libraries from the entomopathogenic fungus Beauveria (Cordyceps) bassiana. I. Evidence for stage-specific gene expression in aerial conidia, in vitro blastospores and submerged conidia. Microbiology. 152:2843–2854. doi:https://doi.org/10.1099/mic.0.28844-0.
   PubMedGoogle Scholar
• Chong-Rodríguez MJ, Maldonado-Blanco MG, Hernández-Escareño JJ, Galán-Wong LJ, Sandoval-Coronado CF. 2011. Study of Beauveria bassiana growth, blastospore yield, desiccation-tolerance, viability and toxic activity using different liquid media. Afr J Biotechnol. 10:5736–5742.
   Google Scholar
• Di Bonaventura G, Pompilio A, Picciani C, Lezzi M, D’Antonio D, Piccolomini R. 2006. Biofilm formation by the emerging fungal pathogen Trichosporon asahii: development, architecture, and antifungal resistance. Antimicrob Agents Chemother. 50:3269–3276. doi:https://doi.org/10.1128/AAC.00556-06.
   PubMed Web of Science ®Google Scholar
• Donlan RM. 2001. Biofilm formation: a clinically relevant microbiological process. Clin Infect Dis. 33:1387–1392. doi:https://doi.org/10.1086/322972.
   PubMed Web of Science ®Google Scholar
• Douglas HW, Collins AE, Parkinson D. 1959. Electric charge and other surface properties of some fungal spores. Biochim Biophys Acta. 33:535–538. doi:https://doi.org/10.1016/0006-3002(59)90145-3.
   PubMed Web of Science ®Google Scholar
• Eisenman HC, Casadevall A. 2012. Synthesis and assembly of fungal melanin. Appl Microbiol Biot. 93:931–940. doi:https://doi.org/10.1007/s00253-011-3777-2.
   PubMed Web of Science ®Google Scholar
• Fanning S, Mitchell AP. 2012. Fungal biofilms. PLoS Pathog. 8(4):e1002585. doi:https://doi.org/10.1371/journal.ppat.1002585.
   PubMed Web of Science ®Google Scholar
• Ferguson CM, Barratt BI, Bell N, Goldson SL, Hardwick S, Jackson T, Phillips C, Popay A, Rennie G, Sinclair S, et al. 2019. Quantifying the economic cost of invertebrate pests to New Zealand’s pastoral industry. New Zeal J Agr Res. 62:255–315. doi:https://doi.org/10.1080/00288233.2018.1478860.
   Web of Science ®Google Scholar
• Griffiths D. 1970. The fine structure of developing microsclerotia of Verticillium dahliae Kleb. Arch Microbiol. 74:207–212.
   Google Scholar
• Grijalba EP, Espinel C, Cuartas P, Chaparro M, Villamizar L. 2018. Metarhizium rileyi biopesticide to control Spodoptera frugiperda: stability and insecticidal activity under glasshouse conditions. Fungal Biol. 122:1069–1076. doi:https://doi.org/10.1016/j.funbio.2018.08.010.
   PubMed Web of Science ®Google Scholar
• Holder DJ, Keyhani NO. 2005. Adhesion of the entomopathogenic fungus Beauveria (Cordyceps) bassiana to substrata. Appl Environ Microbiol. 71:5260–5266. doi:https://doi.org/10.1128/AEM.71.9.5260-5266.2005.
   PubMed Web of Science ®Google Scholar
• Huarte‐Bonnet C, Paixão FR, Mascarin GM, Santana M, ÉK F, Pedrini N. 2019. The entomopathogenic fungus Beauveria bassiana produces microsclerotia‐like pellets mediated by oxidative stress and peroxisome biogenesis. Environ Microbiol Rep. doi:https://doi.org/10.1111/1758-2229.12742
   Google Scholar
• Jackson MA, Jaronski ST. 2009. Production of microsclerotia of the fungal entomopathogen Metarhizium anisopliae and their potential for use as a biocontrol agent for soil-inhabiting insects. Mycol Res. 113:842–850. doi:https://doi.org/10.1016/j.mycres.2009.03.004.
   PubMed Web of Science ®Google Scholar
• Jaronski ST, Jackson MA. 2008. Efficacy of Metarhizium anisopliae microsclerotia granules. Biocontrol Sci Tech. 18:849–863. doi:https://doi.org/10.1080/09583150802381144.
   Web of Science ®Google Scholar
• Jaronski ST, Jackson MA. 2009. Further progress with Metarhizium microsclerotial production. IOBC/WPRS Bulletin. 45:275–278.
   Google Scholar
• Jaronski ST, Jackson MA. 2012. Mass production of entomopathogenic Hypocreales. In: Lacey L, editor. Manual of Techniques in Invertebrate Pathology. 2nd ed. London (UK): Academic Press; p. 255–284.
   Google Scholar
• Jaronski ST, Mascarin GM. 2016. Mass production of fungal entomopathogens. In: Lacey LA, editor. Microbial control of insect and mite pests: from theory to practice. First ed. Elsevier, Amsterdam, Academic Press; p. 141–155.
   Google Scholar
• Kernien JF, Snarr BD, Sheppard DC, Nett JE. 2018. The interface between fungal biofilms and innate immunity. Front Immunol. 8:1968. doi:https://doi.org/10.3389/fimmu.2017.01968.
   PubMed Web of Science ®Google Scholar
• Kobori NN, Mascarin GM, Jackson MA, Schisler DA. 2015. Liquid culture production of microsclerotia and submerged conidia by Trichoderma harzianum active against damping-off disease caused by Rhizoctonia solani. Fungal Biol. 119:179–190. doi:https://doi.org/10.1016/j.funbio.2014.12.005.
   PubMed Web of Science ®Google Scholar
• Kumar R, Saraswat D, Tati S, Edgerton M. 2015. Novel aggregation properties of Candida albicans secreted aspartyl proteinase sapVI mediate virulence in oral candidiasis. Infect Immun. 83:2614–2626. doi:https://doi.org/10.1128/IAI.00282-15.
   PubMed Web of Science ®Google Scholar
• Lagree K, Desai JV, Finkel JS, Lanni F. 2018. Microscopy of fungal biofilms. Curr Opin Microbiol. 43:100–107. doi:https://doi.org/10.1016/j.mib.2017.12.008.
   PubMedGoogle Scholar
• Lohse R, Jakobs-Schönwandt D, Patel AV. 2014. Screening of liquid media and fermentation of an endophytic Beauveria bassiana strain in a bioreactor. AMB Express. 4:47. doi:https://doi.org/10.1186/s13568-014-0047-6.
   PubMedGoogle Scholar
• Mansfield S, Gerard PJ, Hurst MRH, Townsend RJ, Wilson DJ, van Koten C. 2016. Dispersal of the invasive pasture pest Heteronychus arator into areas of low population density: effects of sex and season, and implications for pest management. Front Plant Sci. doi:https://doi.org/10.3389/fpls.2016.01278
   Google Scholar
• Mitchell KF, Zarnowski R, Andes DR. 2016. The extracellular matrix of fungal biofilms. In: Imbert C, editor. Fungal biofilms and related infections. Advances in experimental medicine and biology, Vol. 931. New York: Springer Nature; p. 21–35.
   Google Scholar
• Nagy E. 2002. Three-phase oxygen absorption and its effect on fermentation. In: Dutta NN, editor. History and trends in bioprocessing and biotransformation. Heidelberg: Springer; p. 51–80.
   Google Scholar
• Nicholson RL, Moraes WB. 1980. Survival of Colletotrichum graminicola: importance of the spore matrix. Phytopathology. 70:255–261. doi:https://doi.org/10.1094/Phyto-70-255.
   Web of Science ®Google Scholar
• Noor R. 2015. Mechanism to control the cell lysis and the cell survival strategy in stationary phase under heat stress. Springerplus. 4:599. doi:https://doi.org/10.1186/s40064-015-1415-7.
   PubMedGoogle Scholar
• Nosanchuk JD, Casadevall A. 2003. The contribution of melanin to microbial pathogenesis. Cellular Microbiology. 5(4):203–223. doi:https://doi.org/10.1046/j.1462-5814.2003.00268.x.
   PubMed Web of Science ®Google Scholar
• Peiqian L, Xiaoming P, Huifang S, Jingxin Z, Ning H, Birun L. 2014. Biofilm formation by Fusarium oxysporum f. sp. cucumerinum and susceptibility to environmental stress. FEMS Microbiol Lett. 350:138–145. doi:https://doi.org/10.1111/1574-6968.12310.
   PubMed Web of Science ®Google Scholar
• Ramage G, Mowat E, Jones B, Williams C, Lopez-Ribot J. 2009. Our current understanding of fungal biofilms. Crit Rev Microbiol. 35:340–355. doi:https://doi.org/10.3109/10408410903241436.
   PubMed Web of Science ®Google Scholar
• Ravensberg WJ. 2011. A roadmap to the successful development and commercialization of microbial pest control products for control of arthropods.Vol. 10, progress in biological control. Dordrecht: Springer Science + Business Media B.V.
   Google Scholar
• Reynolds ES. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 17:208. doi:https://doi.org/10.1083/jcb.17.1.208.
   PubMed Web of Science ®Google Scholar
• Schisler DA, Jackson MA. 1996. Germination of soil-incorporated microsclerotia of Colletotrichum truncatum and colonization of seedlings of the weed Sesbania exaltata. Can J Microbiol. 42:1032–1038. doi:https://doi.org/10.1139/m96-132.
   Google Scholar
• Shearer JF, Jackson MA. 2006. Liquid culturing of microsclerotia of Mycoleptodiscus terrestris, a potential biological control agent for the management of Hydrilla. Biol Control. 38:298–306. doi:https://doi.org/10.1016/j.biocontrol.2006.04.012.
   Web of Science ®Google Scholar
• Sheppard DC, Howell PL. 2016. Biofilm exopolysaccharides of pathogenic fungi: lessons from bacteria. J Biol Chem. 291:12529–12537. doi:https://doi.org/10.1074/jbc.R116.720995.
   PubMed Web of Science ®Google Scholar
• Soesanto L, Termorshuizen AJ. 2001. Effect of Temperature on the Formation of Microsclerotia of Verticillium dahliae. J Phytopathol. 149:685–691. doi:https://doi.org/10.1046/j.1439-0434.2001.00697.x.
   Google Scholar
• Song Z. 2018. Fungal microsclerotia development: essential prerequisites, influencing factors, and molecular mechanism. Appl Microbiol Biotechnol. 102:9873–9880. doi:https://doi.org/10.1007/s00253-018-9400-z.
   PubMedGoogle Scholar
• Song Z, Lin Y, Du F, Yin Y, Wang Z. 2017. Statistical optimisation of process variables and large-scale production of Metarhizium rileyi (Ascomycetes: hypocreales) microsclerotia in submerged fermentation. Mycology. 8:39–47. doi:https://doi.org/10.1080/21501203.2017.1279688.
   Google Scholar
• Song Z, Shen L, Zhong Q, Yin Y, Wang Z. 2016. Liquid culture production of microsclerotia of Purpureocillium lilacinum for use as bionematicide. Nematology. 18:719–726. doi:https://doi.org/10.1163/15685411-00002987.
   Web of Science ®Google Scholar
• Song ZY, Yin YP, Jiang SS, Liu JJ, Wang ZK. 2014. Optimization of culture medium for microsclerotia production by Nomuraea rileyi and analysis of their viability for use as a mycoinsecticide. BioControl. 59:597–605. doi:https://doi.org/10.1007/s10526-014-9589-4.
   Web of Science ®Google Scholar
• Varo A, Raya‐Ortega M, Trapero A. 2016. Enhanced production of microsclerotia in recalcitrant Verticillium dahliae isolates and its use for inoculation of olive plants. J Appl Microbiol. 121:473–484. doi:https://doi.org/10.1111/jam.13167.
   PubMedGoogle Scholar
• Veiter L, Rajamanickam V, Herwig C. 2018. The filamentous fungal pellet—relationship between morphology and productivity. Appl Microbiol Biotechnol. 102:2997–3006. doi:https://doi.org/10.1007/s00253-018-8818-7.
   PubMed Web of Science ®Google Scholar
• Villamizar LF, Nelson TL, Jones SA, Jackson TA, Hurst MR, Marshall SD. 2018. Formation of microsclerotia in three species of eauveria and storage stability of a prototype granular formulation. Biocontrol Sci Tech. 28:1097–1113. doi:https://doi.org/10.1080/09583157.2018.1514584.
   Web of Science ®Google Scholar
• Wang HH, Wang JL, Li YP, Liu X, Wen JZ, Lei ZR. 2011. Liquid culturing of microsclerotia of Beauveria bassiana, an entomopathogenic fungus to control western flower thrip, Frankliniella occidentalis. Chin J Appl Entomol. 48:588–595.
   Google Scholar
• Weisberg SH, Turian G. 1974. The membraneous type of lomasome (membranosome) in the hyphae of Aspergillus nidulans. Protoplasma. 79::377–389. doi:https://doi.org/10.1007/BF01276612.
   Google Scholar
• Wilsenach R, Kessel M. 1965. The role of lomasomes in wall formation in Penicillium vermiculatum. Microbiology. 40::401–404.
   Web of Science ®Google Scholar
• Zar J 1999. Biostatistical analysis, cuarta Ed. ed. New Jersey.
   Google Scholar
• Zhang J, Zhang J. 2016. The filamentous fungal pellet and forces driving its formation. Crit Rev Biotechnol. 36:1066–1077. doi:https://doi.org/10.3109/07388551.2015.1084262.
   PubMed Web of Science ®Google Scholar