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Comparison between superficial and solid-state cultures of Isaria fumosorosea: conidial yields, quality and sensitivity to oxidant conditions

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Abstract

Conidia production and quality from mycoinsecticides in solid-state cultures (SSC) are frequently inferred from superficial culture (SC) results. Both parameters were evaluated for two Isaria fumosorosea strains (ARSEF 3302 and CNRCB1), in SC and SSC, using culture media with the same chemical composition. For both strains, conidia production was higher in SC than SSC in terms of conidia per gram of dry substrate. Germination in both strains did not show significant differences between SC and SSC (>90 %). Similarly, conidia viability in ARSEF 3302 strain did not show differences at early stages between SC and SSC, but was higher in SC compared to SSC in the late stage of culture; in contrast, conidia from CNRCB1 strain did not differ between both culture systems. Some infectivity parameters improved in conidia from SSC, compared to SC at the early stages, but these differences disappeared at the final stage, independently of the strain. Both strains showed decreased conidia production when 26 % O2 pulses were applied; nevertheless, conidiation in SSC was two orders of magnitude more sensitive to oxidant pulses. In SC with 26 % O2 pulses, conidia viability for both strains at early stages, was higher than in normal atmospheric conditions. Infectivity towards Galleria mellonella larvae was similar between conidia from normal atmosphere and oxidant conditions; notably, for the strain ARSEF 3302 infectivity decreased at the final stage. This study shows the intrinsic differences between SC and SSC, which should be considered when using SC as a model to design production processes in SSC.

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References

  • Allen MT, Levy LS (2013) Parkinson’s disease and pesticide exposure—a new assessment. Crit Rev Toxicol 43:515–534. doi:10.3109/10408444.2013.798719

    Article  CAS  Google Scholar 

  • Altre JA, Vandenberg JD, Cantone FA (1999) Pathogenicity of Paecilomyces fumosoroseus Isolates to Diamondback Moth, Plutella xylostella: correlation with spore size, germination speed, and attachment to cuticle. J Invertebr Pathol 73:332–338. doi:10.1006/jipa.1999.4844

    Article  CAS  Google Scholar 

  • Batta YA (2007) Biocontrol of almond bark beetle (Scolytus amygdali Geurin-Meneville, Coleoptera: Scolytidae) using Beauveria bassiana (Bals.) Vuill. (Deuteromycotina: Hyphomycetes). J Appl Microbiol 103:1406–1414. doi:10.1111/j.1365-2672.2007.03369.x

    Article  CAS  Google Scholar 

  • Behle RW, Garcia-Gutierrez C, Tamez-Guerra P, McGuire MR, Jackson MA (2006) Pathogenicity of blastospores and conidia of Paecilomyces fumosoroseus against larvae of the Mexican bean beetle, Epilachna varivestis Mulsant. Southwest Entomol 31:289–295

    Google Scholar 

  • Boguś MI, Kędra E, Bania J, Szczepanik M, Czygier M, Jabłoński P, Pasztaleniec A, Samborski J, Mazgajska J, Polanowski A (2007) Different defense strategies of Dendrolimus pini, Galleria mellonella, and Calliphora vicina against fungal infection. J Insect Physiol 53:909–922. doi:10.1016/j.jinsphys.2007.02.016

    Article  Google Scholar 

  • Cliquet S, Jackson MA (2005) Impact of carbon and nitrogen nutrition on the quality, yield and composition of blastospores of the bioinsecticidal fungus Paecilomyces fumosoroseus. J Ind Microbiol Biotechnol 32:204–210. doi:10.1007/s10295-005-0232-3

    Article  CAS  Google Scholar 

  • Favela-Torres E, Cordova-Lopez J, García-Rivero M, Gutiérrez-Rojas M (1998) Kinetics of growth of Aspergillus niger during submerged, agar surface and solid state fermentations. Process Biochem 33:103–107. doi:10.1016/S0032-9592(97)00032-0

    Article  CAS  Google Scholar 

  • Garcia-Ortiz N, Tlecuitl-Beristain S, Favela-Torres E, Loera O (2015) Production and quality of conidia by Metarhizium anisopliae var. lepidiotum: critical oxygen level and period of mycelium competence. Appl Microbiol Biotechnol 99:2783–2791. doi:10.1007/s00253-014-6225-2

    Article  CAS  Google Scholar 

  • Garza-López PM, Konigsberg M, Saucedo-Castaneda G, Loera O (2011) Differential profiles of Beauveria bassiana (Bals.-Criv.) Vuill. as a response to CO2: production of conidia and amylases. Agrociencia 45:761–770

    Google Scholar 

  • Garza-López PM, Konigsberg M, Gómez-Quiroz LE, Loera O (2012) Physiological and antioxidant response by Beauveria bassiana Bals (Vuill.) to different oxygen concentrations. World J Microb Biotechnol 28:353–359. doi:10.1007/s11274-011-0827-y

    Article  Google Scholar 

  • Hansberg W, De Groot H, Sies H (1993) Reactive oxygen species associated with cell differentiation in Neurospora crassa. Free Radic Bio Med 14:287–293. doi:10.1016/0891-5849(93)90025-P

    Article  CAS  Google Scholar 

  • Hegedus DD, Bidochka MJ, Miranpuri GS, Khachatourians GG (1992) A comparison of the virulence, stability and cell-wall-surface characteristics of three spore types produced by the entomopathogenic fungus Beauveria bassiana. Appl Microbiol Biotechnol 36:785–789. doi:10.1007/BF00172195

    Article  Google Scholar 

  • Hunter WB, Avery PB, Pick D, Powell CA (2011) Broad spectrum potential of Isaria fumosorosea against insect pests of citrus. Fla Entomol 94:1051–1054. doi:10.1653/024.094.0444

    Article  Google Scholar 

  • Ibrahim L, Butt TM, Jenkinson P (2002) Effect of artificial culture media on germination, growth, virulence and surface properties of the entomopathogenic hyphomycete Metarhizium anisopliae. Mycol Res 106:705–715. doi:10.1017/S0953756202006044

    Article  Google Scholar 

  • James RR, Buckner JS, Freeman TP (2003) Cuticular lipids and silverleaf whitefly stage affect conidial germination of Beauveria bassiana and Paecilomyces fumosoroseus. J Invertebr Pathol 84:67–74. doi:10.1016/j.jip.2003.08.006

    Article  CAS  Google Scholar 

  • Jaronski ST, Jackson MA (2012) Mass production of entomopathogenic Hypocreales. In: Lacey LA (ed) Manual of techniques in invertebrate pathology, 2nd edn. Academic Press, New York, pp 255–284

    Chapter  Google Scholar 

  • Jenkins NE, Grzywacz D (2000) Quality control of fungal and viral biocontrol agents-assurance of product performance. Biocontrol Sci Technol 10:753–777. doi:10.1080/09583150020011717

    Article  Google Scholar 

  • Kamp AM, Bidochka MJ (2002) Conidium production by insect pathogenic fungi on commercially available agars. Lett Appl Microbiol 35:74–77. doi:10.1046/j.1472-765X.2002.01128.x

    Article  CAS  Google Scholar 

  • Lacey LA, Kirk AA, Millar L, Mercadier G, Vidal C (1999) Ovicidal and larvicidal activity of conidia and blastospores of Paecilomyces fumosoroseus (Deuteromycotina: Hyphomycetes) against Bemisia argentifolii (Homoptera: Aleyrodidae) with a description of a bioassay system allowing prolonged survival of control insects. Biocontrol Sci Technol 9:9–18. doi:10.1080/09583159929866

    Article  Google Scholar 

  • Lai T, Su J (2011) Assessment of resistance risk in Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) to chlorantraniliprole. Pest Manag Sci 67:1468–1472. doi:10.1002/ps.2201

    Article  CAS  Google Scholar 

  • Lara-Ortíz T, Riveros-Rosas H, Aguirre J (2003) Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol Microbiol 50:1241–1255. doi:10.1046/j.1365-2958.2003.03800.x

    Article  Google Scholar 

  • López M, Loera O, Guerrero-Olazarán M, Viader-Salvadó JM, Gallegos-López JA, Fernández FJ, Favela-Torres E, Viniegra-González G (2010) Cell growth and Trametes versicolor laccase production in transformed Pichia pastoris cultured by solid-state or submerged fermentations. J Chem Technol Biotechnol 85:435–440. doi:10.1002/jctb.2306

    Google Scholar 

  • López-Pérez M, Rodríguez-Gómez D, Loera O (2014) Production of conidia of Beauveria bassiana in solid-state culture: current status and future perspectives. Crit Rev Biotechnol. doi:10.3109/07388551.2013.857293

    Google Scholar 

  • Mascarin GM, Alves SB, Lopes RB (2010) Culture media selection for mass production of Isaria fumosorosea and Isaria farinosa. Braz Arch Biol Technol 53:753–761. doi:10.1590/S1516-89132010000400002

    Article  Google Scholar 

  • Miranda-Hernández F, Saucedo-Castañeda G, Alatorre-Rosas R, Loera O (2014) Oxygen-rich culture conditions enhance the conidial infectivity and the quality of two strains of Isaria fumosorosea for potentially improved biocontrol processes. Pest Manag Sci 70:661–666. doi:10.1002/ps.3605

    Article  Google Scholar 

  • Montesinos-Matías R, Viniegra-González G, Alatorre-Rosas R, Loera O (2011) Relationship between virulence and enzymatic profiles in the cuticle of Tenebrio molitor by 2-deoxy-d-glucose-resistant mutants of Beauveria bassiana (Bals.) Vuill. World J Microb Biotechnol 27:2095–2102. doi:10.1007/s11274-011-0672-z

    Article  Google Scholar 

  • Morales-Hernández CE, Padilla-Guerrero IE, Hernández GA, Salazar-Solis E, Torres-Guzman JC (2010) Catalase overexpression reduces the germination time and increases the pathogenicity of the fungus Metarhizium anisopliae. Appl Microbiol Biotechnol 87:1033–1044. doi:10.1007/s00253-010-2517-3

    Article  Google Scholar 

  • Murillo-Alonso KT, Peña-Chora G, Hernández-Baltazar E, Hernández-Velázquez VM (2015) Conidia production by Isaria fumosorosea on solid substrates and its pathogenicity towards Bemisia tabaci. Biocontrol Sci Technol 25:175–184. doi:10.1080/09583157.2014.966649

    Article  Google Scholar 

  • Nuñez-Gaona O, Saucedo-Castañeda G, Alatorre-Rosas R, Loera O (2010) Effect of moisture content and inoculum on the growth and conidia production by Beauveria bassiana on wheat bran. Braz Arch Biol Technol 53:771–777. doi:10.1590/S1516-89132010000400004

    Article  Google Scholar 

  • Ortega-Sánchez E, Loera O, Viniegra-González G (2012) The effect of the ratio between substrate concentration and specific area of the support on the biomass yield of fungal surface cultures. Rev Mex Ing Quim 11:485–494

    Google Scholar 

  • Pham TA, Kim JJ, Kim K (2010) Optimization of solid-state fermentation for improved conidia production of Beauveria bassiana as a mycoinsecticide. Mycobiology 38:137–143. doi:10.4489/MYCO.2010.38.2.137

    Article  CAS  Google Scholar 

  • Rahardjo YS, Jolink F, Haemers S, Tramper J, Rinzema A (2005) Significance of bed porosity, bran and specific surface area in solid-state cultivation of Aspergillus oryzae. Biomol Eng 22:133–139. doi:10.1016/j.bioeng.2005.05.002

    Article  CAS  Google Scholar 

  • Rodriguez-Gomez D, Marcial-Quino J, Loera O (2015) Modulation of conidia production and expression of the gene bbrgs1 from Beauveria bassiana by oxygen pulses and light. J Invertebr Pathol 130:82–87. doi:10.1016/j.jip.2015.07.004

    Article  CAS  Google Scholar 

  • Rodríguez-Gómez D, Loera O, Saucedo-Castañeda G, Viniegra-González G (2009) Substrate influence on physiology and virulence of Beauveria bassiana acting on larvae and adults of Tenebrio molitor. World J Microb Biotechnol 25:513–518. doi:10.1007/s11274-008-9917-x

    Article  Google Scholar 

  • Samuels KDZ, Heale JB, Llewellyn M (1989) Characteristics relating to the pathogenicity of Metarhizium anisopliae toward Nilaparvata lugens. J Invertebr Pathol 53:25–31. doi:10.1016/0022-2011(89)90070-0

    Article  Google Scholar 

  • Sánchez-Murillo RI, de la Torre-Martínez M, Aguirre-Linares J, Herrera-Estrella A (2004) Light-regulated asexual reproduction in Paecilomyces fumosoroseus. Microbiology 150:311–319. doi:10.1099/mic.0.26717-0

    Article  Google Scholar 

  • Sargent ML, Kaltenborn SH (1972) Effects of medium composition and carbon dioxide on circadian conidiation in Neurospora. Plant Physiol 50:171–175. doi:10.1104/pp.50.1.171

    Article  CAS  Google Scholar 

  • Shim SM, Lee KR, Kim SH, Im KH, Kim JW, Lee UY, Shim JO, Lee MW, Lee TS (2003) The optimal culture conditions affecting the mycelial growth and fruiting body formation of Paecilomyces fumosoroseus. Mycobiology 31:214–220. doi:10.4489/MYCO.2005.33.1.065

    Article  CAS  Google Scholar 

  • Smalling KL, Kuivila KM, Orlando JL, Phillips BM, Anderson BS, Siegler K, Hunt JW, Hamilton M (2013) Environmental fate of fungicides and other current-use pesticides in a central California estuary. Mar Pollut Bull 73:144–153. doi:10.1016/j.marpolbul.2013.05.028

    Article  CAS  Google Scholar 

  • Sun X, Zhang H, Zhang Z, Wang Y, Li S (2011) Involvement of a helix–loop–helix transcription factor CHC-1 in CO2-mediated conidiation suppression in Neurospora crassa. Fungal Genet Biol 48:1077–1086. doi:10.1016/j.fgb.2011.09.003

    Article  CAS  Google Scholar 

  • Tlecuitl-Beristain S, Viniegra-González G, Díaz-Godínez G, Loera O (2010) Medium selection and effect of higher oxygen concentration pulses on Metarhizium anisopliae var. lepidiotum conidial production and quality. Mycopathologia 169:387–394. doi:10.1007/s11046-009-9268-7

    Article  CAS  Google Scholar 

  • Wyss GS, Charudattan R, DeValerio JT (2001) Evaluation of agar and grain media for mass production of conidia of Dactylaria higginsii. Plant Dis 85:1165–1170. doi:10.1094/PDIS.2001.85.11.1165

    Article  Google Scholar 

  • Ye SD, Ying SH, Chen C, Feng MG (2006) New solid-state fermentation chamber for bulk production of aerial conidia of fungal biocontrol agents on rice. Biotechnol Lett 28:799–804. doi:10.1007/s10529-006-9004-z

    Article  CAS  Google Scholar 

  • Zhang S, Xia YX, Kim B, Keyhani NO (2011) Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development and pathogenesis in the entomopathogenic fungus, Beauveria bassiana. Mol Microbiol 80:811–826. doi:10.1111/j.1365-2958.2011.07613.x

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank the National Council for Science and Technology (CONACyT) for the scholarship granted to F. Muñiz-Paredes (248618) and for the project CB-2010-01-152420; and also the Universidad Autónoma Metropolitana (UAM).

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  1. Departamento de Biotecnología, Universidad Autónoma Metropolitana Iztapalapa, 09340, Iztapalapa, Mexico City, Mexico

    Facundo Muñiz-Paredes, Gustavo Viniegra-González & Octavio Loera

  2. Instituto de Ciencias Agropecuarias, Universidad Autónoma del Estado de Hidalgo, 43600, Tulancingo, Hidalgo, Mexico

    Paul Misael Garza-López

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  1. Facundo Muñiz-Paredes
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  2. Paul Misael Garza-López
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  3. Gustavo Viniegra-González
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Correspondence to Octavio Loera.

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Muñiz-Paredes, F., Garza-López, P.M., Viniegra-González, G. et al. Comparison between superficial and solid-state cultures of Isaria fumosorosea: conidial yields, quality and sensitivity to oxidant conditions. World J Microbiol Biotechnol 32, 111 (2016). https://doi.org/10.1007/s11274-016-2072-x

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