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Glucose concentration alters dissolved oxygen levels in liquid cultures of Beauveria bassiana and affects formation and bioefficacy of blastospores

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Abstract

The filamentous fungus Beauveria bassiana is an economically important pathogen of numerous arthropod pests and is able to grow in submerged culture as filaments (mycelia) or as budding yeast-like blastospores. In this study, we evaluated the effect of dissolved oxygen and high glucose concentrations on blastospore production by submerged cultures of two isolates of B. bassiana, ESALQ1432 and GHA. Results showed that maintaining adequate dissolved oxygen levels coupled with high glucose concentrations enhanced blastospore yields by both isolates. High glucose concentrations increased the osmotic pressure of the media and coincided with higher dissolved oxygen levels and increased production of significantly smaller blastospores compared with blastospores produced in media with lower concentrations of glucose. The desiccation tolerance of blastospores dried to less than 2.6 % moisture was not affected by the glucose concentration of the medium but was isolate dependent. Blastospores of isolate ESALQ1432 produced in media containing 140 g glucose L−1 showed greater virulence toward whitefly nymphs (Bemisia tabaci) as compared with blastospores produced in media containing 40 g glucose L−1. These results suggest a synergistic effect between glucose concentration and oxygen availability on changing morphology and enhancing the yield and efficacy of blastospores of B. bassiana, thereby facilitating the development of a cost-effective production method for this blastospore-based bioinsecticide.

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References

  • Babazadeh R, Adiels CB, Smedh M, Petelenz-Kurdziel E, Goksör M, Hohmann S (2013) Osmostress-induced cell volume loss delays yeast Hog1 signaling by limiting diffusion processes and by Hog1-specific effects. PLoS ONE 8(11), e80901. doi:10.1371/journal.pone.0080901

    Article  PubMed Central  PubMed  Google Scholar 

  • Bewick V, Cheek L, Ball J (2004) Statistics review 12: survival analysis. Crit Care 8:389–394. doi:10.1186/cc2955

    Article  PubMed Central  PubMed  Google Scholar 

  • Bidochka MJ, Pfeifer TA, Khachatourians GG (1987) Development of the entomopathogenic fungus Beauveria bassiana in liquid cultures. Mycopathologia 4:77–83. doi:10.1007/BF00436909

    Article  Google Scholar 

  • Chapman RF (2013) The insects: structure and function, 5th edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Chong-Rodriguez MJ, Maldonado-Blanco MG, Hernandez-Escareno JJ, Galan-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. doi:10.5897/AJB10.2264

    Google Scholar 

  • Duran R, Cary JW, Calvo AM (2011) Role of the osmotic stress regulatory pathway in morphogenesis and secondary metabolism in filamentous fungi. Toxins 2:367–381. doi:10.3390/toxins2040367

    Article  Google Scholar 

  • Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256. doi:10.1016/j.biocontrol.2007.08.001

    Article  Google Scholar 

  • Feng MG, Poprawski TJ, Khachatourians GG (1994) Production, formulation and application of the entomopathogenic fungus Beauveria bassiana for insect control: current status. Biocontrol Sci Techn 4:3–34. doi:10.1080/09583159409355309

    Article  Google Scholar 

  • Giese H, Azizan A, Kümmel A, Liao A, Peter CP, Fonseca JA, Hermann R, Duarte TM, Büches J (2013) Liquid films on shake flask walls explain increasing maximum oxygen transfer capacities with elevating viscosity. Biotechnol Bioeng 111:295–308. doi:10.1002/bit.25015

    Article  PubMed  Google Scholar 

  • Hohmann S (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol R 66:300–372. doi:10.1128/MMBR.66.2.300-372.2002

    Article  CAS  Google Scholar 

  • Humber RA (2008) Evolution of entomopathogenicity in fungi. J Invertebr Pathol 98:262–266. doi:10.1016/j.jip.2008.02.017

    Article  PubMed  Google Scholar 

  • Humphreys AM, Matewele P, Trinci APJ (1989) Effects of water activity on morphology, growth and blastospore production of Metarhizium anisopliae, Beauveria bassiana and Paecilomyces farinosus in batch and fed-batch culture. Mycol Res 92:257–264. doi:10.1080/09583150400016910

    Article  Google Scholar 

  • Inch JM, Trinci APJ (1987) Effects of water activity on growth and sporulation of Paecilomyces farinosus in liquid and solid media. J Gen Microbiol 113:247–252. doi:10.1099/00221287-133-2-247

    Google Scholar 

  • Issaly N, Chauveau H, Aglevor F, Fargues J, Durand A (2005) Influence of nutrient, pH and dissolved oxygen on the production of Metarhizium flavoviridae Mf189 blastospores in submerged batch culture. Process Biochem 40:1425–1431. doi:10.1016/j.procbio.2004.06.029

    Article  CAS  Google Scholar 

  • Jackson MA (1997) Optimizing nutritional conditions for the liquid culture production of effective fungal biological control agents. J Ind Microbiol Biotechnol 19:180–187. doi:10.1038/sj.jim.2900426

    Article  CAS  Google Scholar 

  • Jackson MA (2012) Dissolved oxygen levels affect dimorphic growth by the entomopathogenic fungus Isaria fumosorosea. Biocontrol Sci Technol 22:67–79. doi:10.1080/09583157.2011.642339

    Article  Google Scholar 

  • Jackson MA, Payne AR (2007) Evaluation of the desiccation tolerance of blastospores of Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) using a lab-scale, air-drying chamber with controlled relative humidity. Biocontrol Sci Technol 17:709–719. doi:10.1080/09583150701527235

  • Jackson MA, McGuire MR, Lacey LA, Wraight SP (1997) Liquid culture production of desiccation tolerant blastospores of the bioinsecticidal fungus Paecilomyces fumosoroseus. Mycol Res 101:35–41. doi:10.1017/S0953756296002067

    Article  Google Scholar 

  • Jackson MA, Cliquet S, Iten LB (2003) Media and fermentation process for the rapid production of high concentrations of stable blastospores of the bioinsecticidal fungus Paecilomyces fumosoroseus. Biocontrol Sci Technol 13:23–33. doi:10.1080/0958315021000054368

    Article  Google Scholar 

  • Jackson MA, Dunlap CA, Jaronski ST (2010) Ecological considerations in producing and formulating fungal entomopathogens for use in insect biocontrol. BioControl 55:129–145. doi:10.1007/s10526-009-9240-y

    Article  Google Scholar 

  • Kleespies RG, Zimmermann G (1992) Production of blastospores by three strains of Metarhizium anisopliae (Metch.) Sorokin in submerged culture. Biocontrol Sci Technol 2:127–135. doi:10.1080/09583159209355226

    Article  Google Scholar 

  • Lane BL, Trinci PJ, Gillespie AT (1991) Endogenous reserves and survival of blastospores of Beauveria bassiana harvested from carbon- and nitrogen-limited batch cultures. Mycol Res 95:821–828. doi:10.1016/S0953-7562(09)80045-2

    Article  Google Scholar 

  • Li Q, Bai Z, O’Donnell A, Harvey LM, Hoskisson PA, McNeil (2011) Oxidative stress in fungal fermentation processes: the roles of alternative respiration. Biotechnol Lett 33:457–467. doi:10.1007/s10529-010-0471-x

    Article  CAS  PubMed  Google 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:10.1186/s13568-014-0047-6

    Article  PubMed Central  PubMed  Google Scholar 

  • Mascarin GM, Kobori NN, Quintela ED, Delalibera I Jr (2013) The virulence of entomopathogenic fungi against Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) and their conidial production using solid substrate fermentation. Biol Control 66:209–218. doi:10.1016/j.biocontrol.2013.05.001

    Article  Google Scholar 

  • Mascarin GM, Jackson MA, Kobori NN, Behle RW, Delalibera I Jr (2015) Liquid culture fermentation for rapid production of desiccation tolerant blastospores of Beauveria bassiana and Isaria fumosorosea strains. J Invertebr Pathol 127:11–20. doi:10.1016/j.jip.2014.12.001

    Article  CAS  PubMed  Google Scholar 

  • Norrish RS (1966) An equation for the activity and equilibrium relative humidities of water in confectionary syrups. J Food Technol 1:476–484. doi:10.1111/j.1365-2621.1966.tb01027.x

    Google Scholar 

  • Peter CP, Lotter S, Maier U, Büchs J (2004) Impact of out-of-phase conditions on screening results in shaking flask experiments. Biochem Eng J 17:205–215. doi:10.1016/S1369-703X(03)00179-7

    Article  CAS  Google Scholar 

  • Pham TA, Kim JJ, Kim K (2009) Production of blastospore of entomopathogenic Beauveria bassiana in a submerged batch culture. Mycobiology 37:218–224. doi:10.4489/MYCO.2009.37.3.218

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ruiz-Herrera J (1985) Dimorphism in Mucor species with emphasis on M. rouxii and M. bacilliformis. In: Szaniszlo PJ, Harris JL (eds) Fungal dimorphism with emphasis on fungi pathogenic for humans. Springer, New York, USA, pp 361–384

    Google Scholar 

  • Samsinakova A (1966) Growth and sporulation of submerged cultures of the fungus Beauveria bassiana in various media. J Invertebr Pathol 8:395–400. doi:10.1016/0022-2011(66)90056-5

    Article  Google Scholar 

  • Vega FE, Jackson MA, Mercadier M, Poprawski TJ (2003) The impact of nutrition on spore yields for various fungal entomopathogens in liquid culture. World J Microbiol Biotechnol 19:363–368. doi:10.1023/A:1023924304456

    Article  CAS  Google Scholar 

  • Vidal C, Fargues J, Lacey LA, Jackson MA (1998) Effect of various liquid culture media on morphology, growth, propagule production, and pathogenic activity to Bemisia argentifolii of the entomopathogenic hyphomycete, Paecilomyces fumosoroseus. Mycopathologia 143:33–46. doi:10.1023/A:1006962808712

    Article  CAS  Google Scholar 

  • Wanchoo A, Lewis MW, Keyhani NO (2009) Lactin-mapping reveals stage-specific display of surface carbohydrates in in vitro and hemolymph-derived cells of the entomopathogenic fungus Beauveria bassiana. Microbiology 155:3121–3133. doi:10.1099/mic.0.029157-0

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Duan Z, St Leger RJ (2008) MOS1 osmosensor of Metarhizium anisopliae is required for adaptation to insect host hemolymph. Eukaryot Cell 7:302–309. doi:10.1128/EC.00310-07

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang J, Liu J, Hu Y, Ying SH, Feng MG (2013) Cytokinesis-required Cdc14 is a signaling hub of asexual development and multi-stress tolerance in Beauveria bassiana. Sci Rep 3:3086. doi:10.1038/srep03086

    PubMed Central  PubMed  Google Scholar 

  • Wheeler MW, Fadel J, Robertson JK, Bailer J (2007) Confidence interval construction for relative toxicity endpoints such as LD50 or LD90 ratios. J Econ Entomol 100:1945–1949. doi:10.1603/0022-0493(2007)100[1945:CICFRT]2.0.CO;2

    Article  PubMed  Google Scholar 

  • Ypsilos IK, Magan N (2004) Impact of water-stress and washing treatments on production, synthesis and retention of endogenous sugar alcohols and germinability of Metarhizium anisopliae blastospores. Mycol Res 108:1337–1345. doi:10.1017/S0953756204001030

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Brazilian Agricultural Research Corporation (EMBRAPA) for the scholarship to the first author. Special thanks to Dr. Steven P. Arthurs for providing the whitefly founders. We express our sincere gratitude to two anonymous reviewers for their insightful comments on an earlier draft of this article.

Conflict of interest

The authors declare no competing financial interests.

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Authors and Affiliations

  1. EMBRAPA Rice and Beans, Rodovia GO-462, km 12, Zona Rural, C.P. 179, Santo Antônio de Goiás, GO, 75375-000, Brazil

    Gabriel Moura Mascarin

  2. United States Department of Agriculture, Agriculture Research Service, Crop Bioprotection Research Unit, National Center for Agricultural Utilization Research, 1815 N. University St, Peoria, IL, 61604, USA

    Gabriel Moura Mascarin, Mark A. Jackson, Nilce Naomi Kobori, Robert W. Behle & Christopher A. Dunlap

  3. Department of Entomology and Acarology, Escola Superior de Agricultura “Luiz de Queiroz”, University of São Paulo (ESALQ-USP), Av. Pádua Dias, 11, C.P. 9, Piracicaba, SP, 13418-900, Brazil

    Gabriel Moura Mascarin & Ítalo Delalibera Júnior

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  1. Gabriel Moura Mascarin
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  2. Mark A. Jackson
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  4. Robert W. Behle
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Correspondence to Gabriel Moura Mascarin or Mark A. Jackson.

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“Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by EMBRAPA or the U.S. Department of Agriculture. USDA is an equal opportunity provider and Employer”

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Mascarin, G.M., Jackson, M.A., Kobori, N.N. et al. Glucose concentration alters dissolved oxygen levels in liquid cultures of Beauveria bassiana and affects formation and bioefficacy of blastospores. Appl Microbiol Biotechnol 99, 6653–6665 (2015). https://doi.org/10.1007/s00253-015-6620-3

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