Skip to main content
Log in

Production of conidia by entomopathogenic fungi: from inoculants to final quality tests

  • Review
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Demand for biopesticides is growing due to the increase of areas under integrated pest management worldwide. Conidia from entomopathogenic fungi play a major role as infective units in the current market of biopesticides. Success in a massive production of fungal conidia include the use of proper long-term conservation microbial methods, aimed at preserving the phenotypic traits of the strains. The development of suitable inoculants should also be considered since that favours a rapid germination and invasiveness of the substrate in solid state cultures (SSC). After the selection of a suitable fungal strain, proven optimization approaches for SSC mainly include the combination of substrates, moisture, texturizers, aeration and moderate stress to induce conidiation. Nonetheless, during storage and upon application in open fields, conidia either as free propagules or imbibed in formulations are subjected to stress due to abiotic factors, then quality should be preserved to resist such harsh conditions. All of these topics are analysed in this report.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Ali S, Huang Z, Li H, Bashir MH, Ren S (2013) Antioxidant enzyme influences germination, stress tolerance, and virulence of Isaria fumosorosea. J Basic Microbiol 53:489–497. doi:10.1002/jobm.201100645

    Article  CAS  Google Scholar 

  • Amin L, Zainol ZA, Rusly NS, Akpoviri F, Sidik NM (2011) Risk assessment of genetically modified organisms (GMOs). Afr J Biotechnol 58:12418–12424. doi:10.5897/AJB11.1063

    Google Scholar 

  • Angel-Cuapio A, Figueroa-Montero A, Favela-Torres E, Viniegra-Gonzalez G, Perraud-Gaime I, Loera O (2015) Critical values of porosity in rice cultures of Isaria fumosorosea by adding water hyacinth: effect on conidial yields and quality. Appl Biochem Biotechnol 177:446–457. doi:10.1007/s12010-015-1754-4

    Article  CAS  Google Scholar 

  • Ansari MA, Butt TM (2011) Effects of successive subculturing on stability, virulence, conidial yield, germination and shelf-life of entomopathogenic fungi. J Appl Microbiol 110:1460–1469. doi:10.1111/j.1365-2672.2011.04994.x

    Article  CAS  Google Scholar 

  • Arzumanov T, Jenkins N, Roussos S (2005) Effect of aeration and substrate moisture content on sporulation of Metarhizium anisopliae var. acridum. Process Biochem 40:1037–1042. doi:10.1016/j.procbio.2004.03.013

    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 

  • Boas AMV, Andrade RM, Oliveira JV (1996) Diversification of culture media for production of entomopathogenic fungi. Arq Biol Technol 39:123–128

    Google Scholar 

  • Borisade OA, Magan N (2014) Growth and sporulation of entomopathogenic Beauveria bassiana, Metarhizium anisopliae, Isaria farinosa and Isaria fumosorosea strains in relation to water activity and temperature interactions. Biocontrol Sci Technol 24:999–1011. doi:10.1080/09583157.2014.909007

    Article  Google Scholar 

  • Butt TM, Wang C, Shah FA, Hall R (2006) Degeneration of entomopathogenous fungi. In: Eilenberg J, Hokkanen HMT (eds) An ecological and societal approach to biological control. Springer, Netherlands, pp 213–226

    Chapter  Google Scholar 

  • Chantasingh D, Kitikhun S, Keyhani NO, Boonyapakron K, Thoetkiattikul H, Pootanakit K, Eurwilaichitr L (2013) Identification of catalase as an early up-regulated gene in Beauveria bassiana and its role in entomopathogenic fungal virulence. Biol Control 67:85–93. doi:10.1016/j.biocontrol.2013.08.004

    Article  CAS  Google Scholar 

  • Chitarra GS, Abee T, Rombouts FM, Dijksterhuis J (2005) 1-Octen-3-ol inhibits conidia germination of Penicillium paneum despite of mild effects on membrane permeability, respiration, intracellular pH, and changes the protein composition. FEMS Microbiol Ecol 54:67–75. doi:10.1016/j.femsec.2005.02.013

    Article  CAS  Google Scholar 

  • Dalla Santa HS, Sousa NJ, Brand D, Dalla Santa OR, Pandey A, Sobotka M, Paca J, Soccol CR (2004) Conidia production of Beauveria sp. by solid-state fermentation for biocontrol of Ilex paraguariensis caterpillars. Folia Microbiol 49:418–422

    Article  CAS  Google Scholar 

  • Dalla Santa HS, Dalla Santa OR, Brand D, Vandenberghe LPD Soccol CR (2005) Spore production of Beauveria bassiana from agro-industrial residues. Braz Arch Biol Technol 48:51–60. doi:10.1590/S1516-89132005000400007

    Article  Google Scholar 

  • de 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 

  • Fang W, Feng J, Fan Y, Zhang Y, Bidochka MJ, Leger RJS, Pei Y (2009) Expressing a fusion protein with protease and chitinase activities increases the virulence of the insect pathogen Beauveria bassiana. J Invertebr Pathol 102:155–159. doi:10.1016/j.jip.2009.07.013

    Article  CAS  Google Scholar 

  • FAO (2003) Weighing the GMO arguments: against. FAO. http://fao.org/english/newsroom/focus/2003/gmo8.htm. Accessed 22 Sept 2016

  • Farrar JJ, Baur ME, Elliott S (2015) Adoption and impacts of integrated pest management in agriculture in the western United States. Western IPM Center. http://westernipm.org/index.cfm/about-the-center/publications/special-reports/adoption-and-impact-report-abstract/. Accessed 6 Oct 2016

  • Fernandes ÉKK, Rangel DEN, Braga GUL, Roberts DW (2015) Tolerance of entomopathogenic fungi to ultraviolet radiation: a review on screening of strains and their formulation. Curr Genet 61:427–440. doi:10.1007/s00294-015-0492-z

    Article  CAS  Google Scholar 

  • Hallsworth JE, Magan N (1996) Culture age, temperature, and pH affect the polyol and trehalose contents of fungal propagules. Appl Environ Microbiol 62:2435–2442

    CAS  Google Scholar 

  • Herrero-Garcia E, Garzia A, Codobés S, Espeso EA, Ugalde U (2011) 8-Carbon oxylipins inhibit germination and growth, and stimulate aerial conidiation in Aspergillus nidulans. Fungal Biol 115:393–400. doi:10.1016/j.funbio.2011.02.005

    Article  CAS  Google Scholar 

  • Hussain A, Tian MY, He YR, Ruan L, Ahmed S (2010) In vitro and in vivo culturing impacts on the virulence characteristics of serially passed entomopathogenic fungi. J Food Agr Environ 8:481–487

    Google Scholar 

  • Jenkins NE, Heviefo G, Langewald J, Cherry AJ, Lomer CJ (1998) Development of mass production technology for aerial conidia for use as mycopesticides. Biocontrol News Inf 19:21N–31N

    Google Scholar 

  • Kim JJ, Xie L, Han JH, Lee SY (2014a) Influence of additives on the yield and pathogenicity of conidia produced by solid state cultivation of an Isaria javanica isolate. Mycobiology 42:346–352. doi:10.5941/MYCO.2014.42.4.346

    Article  Google Scholar 

  • Kim SY, Kim KH, Im CH, Lee CY, Kong WS, Ryu JS (2014b) Identification of degenerate nuclei and development of a SCAR marker for Flammulina velutipes. PLoS ONE. doi:10.1371/journal.pone.0107207

    Google Scholar 

  • Kooyman C, Godonou I (1997) Infection of Schistocerca gregaria (Orthoptera: Acrididae) hoppers by Metarhizium flavoviride (Deuteromycotina: Hyphomycetes) conidia in an oil formulation applied under desert conditions. Bull Entomol Res 87:105–107

    Article  Google Scholar 

  • Krishna C (2005) Solid-state fermentation systems—an overview. Crit Rev Biotechnol 25:1–30. doi:10.1080/07388550590925383

    Article  CAS  Google Scholar 

  • Li L, Pischetsrieder M, St. Leger RJ, Wang C (2008) Associated links among mtDNA glycation, oxidative stress and colony sectorization in Metarhizium anisopliae. Fugal Genet Biol 45:1300–1306. doi:10.1016/j.fgb.2008.06.003

    Article  CAS  Google Scholar 

  • Li L, Hu X, Xia Y, Xiao G, Zheng P, Wang C (2014) Linkage of oxidative stress and mitochondrial dysfunctions to spontaneous culture degeneration in Aspergillus nidulans. Mol Cell Proteom 13:449–461. doi:10.1074/mcp.M113.028480

    Article  CAS  Google Scholar 

  • Liao X, Lu HL, Fang W, St Leger RJ (2014) Overexpression of a Metarhizium robertsii HSP25 gene increases thermotolerance and survival in soil. Appl Microbiol Biotechnol 98:777–783. doi:10.1007/s00253-013-5360-5

    Article  CAS  Google Scholar 

  • Liu H, Wang P, Hu Y, Zhao G, Liu H, Li Z, Wu H, Wang L, Zheng Z (2015) Optimised fermentation conditions and improved collection efficiency using dual cyclone equipment to enhance fungal conidia production. Biocontrol Sci Technol 25:1011–1023. doi:10.1080/09583157.2015.1025701

    Article  Google Scholar 

  • Lopez-Perez M, Rodriguez-Gomez D, Loera O (2015) Production of conidia of Beauveria bassiana in solid-state culture: current status and future perspectives. Crit Rev Biotechnol 35(3):334–341. doi:10.3109/07388551.2013.857293

    Article  CAS  Google Scholar 

  • Luangsa-Ard J, Houbraken J, van Doom T, Hong SB, Borman AM, Hywel-Jones NL, Samson RA (2011) Purpureocillium, a new genus for the medically important Paecilomyces lilacinus. FEMS Microbiol Lett 321:141–149. doi:10.1111/j.1574-6968.2011.02322.x

    Article  CAS  Google Scholar 

  • Mar TT, Suwannarach N, Lumyong S (2012) Isolation of entomopathogenic fungi from Northern Thailand and their production in cereal grains. World J Microb Biot 28:3281–3291. doi:10.1007/s11274-012-1139-6

    Article  Google Scholar 

  • MarketsAndMarkets (2015) Biopesticides market by type (bioinsecticides, biofungicides, bioherbicides, and bionematicides), origin (beneficial insects, microbials, and biochemical), mode of application, formulation, crop type & region—Global forecast to 2020. MarketsAndMarkets. http://marketsandmarkets.com/Market-Reports/biopesticides-267.html. Accessed 10 Oct 2016

  • Marshall MA, Timberlake WE (1991) Asperillus nidulans wetA activates spore-specific gene expression. Mol Cell Biol 11:55–62. doi:10.1128/EC.00220-13

    Article  CAS  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 

  • Méndez-González F, Loera O, Favela-Torres E (2017) Conidia production of Metarhizium anisopliae in bags and packed column bioreactors. Curr Biotechnol 5:1–5. doi:10.2174/2211550105666160926123350

    Google Scholar 

  • Miranda-Hernández F, Saucedo-Castaneda 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 

  • Miranda-Hernández F, Garza-López PM, Loera O (2016) Cellular signaling in cross protection: an alternative to improve mycopesticides. Biol Control 103:196–203. doi:10.1016/j.biocontrol.2016.09.007

    Article  Google Scholar 

  • Muñiz-Paredes FR, Loera O (2016) The importance of strong inocula in fungal cultures. Mex. J Biotechnol 1(1):120–134

    Google Scholar 

  • Muñiz-Paredes F, Garza-López PM, Viniegra-González G, Loera O (2016) Comparison between superficial and solid-state cultures of Isaria fumosorosea: conidial yields, quality and sensitivity to oxidant conditions. World J Microb Biot 32:111. doi:10.1007/s11274-016-2072-x

    Article  Google Scholar 

  • Nagaraju J, Gopinath G, Sharma V, Shukla JN (2014) Lepidopteran sex determination: a cascade of surprises. Sex Dev 8:104–112. doi:10.1159/000357483

    Article  CAS  Google Scholar 

  • Nemčovič M, Jakubíková L, Víden I, Farkaš V (2008) Induction of conidiation by endogenous volatile compounds in Trichoderma spp. FEMS Microbiol Lett 284:231–236. doi:10.1111/j.1574-6968.2008.01202.x

    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 

  • Ortiz-Urquiza A, Luo Z, Keyhani NO (2015) Improving mycoinsecticides for insect biological control. Appl Microbiol Biotechnol 99:1057–1068. doi:10.1007/s00253-014-6270-x

    Article  CAS  Google Scholar 

  • Pandey A (2003) Solid-state fermentation. Biochem Eng J 13:81–84. doi:10.1016/S1369-703X(02)00121-3

    Article  CAS  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 

  • Prakash GVSB, Padmaja V, Kiran RRS (2008) Statistical, optimization of process variables for the large-scale production of Metarhizium anisopliae conidiospores in solid-state fermentation. Bioresource Technol 99:1530–1537. doi:10.1016/j.biortech.2007.04.031

    Article  CAS  Google Scholar 

  • Pretty J, Bharucha ZP (2015) Integrated pest management for sustainable intensification of agriculture in Asia and Africa. Insects 6:152–182. doi:10.3390/insects6010152

    Article  Google Scholar 

  • Quesada-Moraga F, Vey A (2003) Intra-specific variation in virulence and in vitro production of macromolecular toxins active against locust among Beauveria bassiana strains and effects of in vivo and in vitro passage on these factors. Biocontrol Sci Technol 13:323–340. doi:10.1080/0958315031000110346

    Article  Google Scholar 

  • Rangel DEN (2011) Stress induced cross-protection against environmental challenges on prokaryotic and eukaryotic microbes. World J Microb Biot 27:1281–1296. doi:10.1007/s11274-010-0584-3

    Article  Google Scholar 

  • Rangel DEN, Anderson AJ, Roberts DW (2008) Evaluating physical and nutritional stress during mycelial growth as inducers of tolerance to heat and UV-B radiation in Metarhizium anisopliae conidia. Mycol Res 112:1362–1372. doi:10.1016/j.mycres.2008.04.013

    Article  Google Scholar 

  • Roberts DW, Campbell AS (1977) Stability of entomopathogenic fungi. Misc Publ Entomol Soc Am 10:19–76

    Google Scholar 

  • Ryan MJ, Bridge PD, Smith D, Jeffries P (2002) Phenotypic degeneration occurs during sector formation in Metarhizium anisopliae. J Appl Microbiol 93:163–168. doi:10.1046/j.1365-2672.2002.01682.x

    Article  CAS  Google Scholar 

  • Safavi SA (2012) Attenuation of the entomopathogenic fungus Beauveria bassiana following serial in vitro transfers. Biologia 67:1062–1068. doi:10.2478/s11756-012-0120-z

    Article  Google Scholar 

  • Sahayaraj K, Namasivayam SKR (2008) Mass production of entomopathogenic fungi using agricultural products and by products. Afr J Biotechnol 7:1907–1910

    Article  Google Scholar 

  • Sallam MN (1999) Insect damage. INPhO-Post-harvest Compendium. http://fao.org/3/a-av013e.pdf. Accessed 6 Oct 2016

  • Santoro PH, Zozettti J, Constanski K, Neves PMOJ (2014) Conidial production, virulence and stress tolerance of Beauveria bassiana conidia after successive in vitro subculturing. Rev Colomb Entomol 40:85–90.

    Google Scholar 

  • Sewall TC, Mims CW, Timberlake WE (1990) Conidium differentiation in Aspergillus nidulans wild-type and wet-white (wetA) mutant strains. Dev Biol 138:499–508. doi:10.1016/0012-1606(90)90215-5

    Article  CAS  Google Scholar 

  • Shah FA, Wang CS, Butt TM (2005) Nutrition influences growth and virulence of the insect-pathogenic fungus Metarhizium anisopliae. FEMS Microbiol Lett 251:259–266. doi:10.1016/j.femsle.2005.08.010

    Article  CAS  Google Scholar 

  • Smith C, Edgington S (2011) Germination at different water activities of similarly aged Metarhizium conidia harvested from ageing cultures. J Stored Prod Res 47:157–160. doi:10.1016/j.jspr.2011.01.007

    Article  Google Scholar 

  • Son H, Kim MG, Min K, Lim JY, Choi G, Kim JC, Chae SK, Lee YW (2014) WetA is required for conidiogenesis and conidium maturation in the ascomycete fungus Fusarium graminearum. Eukaryot Cell 13:87–98. doi:10.1128/EC.00220-13

    Article  CAS  Google Scholar 

  • Taylor B, Edgington S, Luke B, Moore D (2013) Yield and germination of the entomopathogenic fungus Beauveria bassiana when grown on different rice preparations. J Stored Prod Res 53:23–26. doi:10.1016/j.jspr.2013.02.004

    Article  Google Scholar 

  • Thaochan N, Chandrapatya A (2016) The phenotypic and metabolic properties of Metarhizium guizhouense on Corcyra cephalonica. Mycosphere 7:214–225. doi:10.5943/mycosphere/7/2/10

    Google Scholar 

  • The BioAg Allience (2016) Fact sheet on the BioAg allience. Monsanto/novozymes. http://monsanto.com/sitecollectiondocuments/bio-ag-alliance-fact-sheet.pdf. Accessed 10 Oct 2016

  • Thomas MB, Jenkins NE (1997) Effects of temperature on growth of Metarhizium flavoviride and virulence to the variegated grasshopper, Zonocerus variegatus. Mycol Res 101:1469–1474. doi:10.1017/S0953756297004401

    Article  Google Scholar 

  • USDA organic regulations (2016) National Organic Program. USDA. http://www.ecfr.gov/cgi-bin/text-idx?SID=bf2cd6c131954f399c05f679321f09ae&mc=true&node=pt7.3.205&rgn=div5#sp7.3.205.c. Accessed 10 Oct 2016

  • Wang C, Butt TM, St Leger RJ (2005) Colony sectorization of Metarhizium anisopliae is a sign of ageing. Microbiology 151:3223–3236. doi:10.1099/mic.0.28148-0

    Article  CAS  Google Scholar 

  • Wang YB, Yang ZH, Yu JJ, Zhang YA, Xue JJ, Zheng L, Li JJ, Wang CY, Wang Z, Hou JG, Begum S, Gu LJ, Lee MR, Sung CK (2013) Comparison between conidia and blastospores of Esteya vermicola, and endoparasitic fungus of the pinewood nematode, Bursaphelenchus xylophilus. World J Microb Biot 29:2429–2436. doi:10.1007/s11274-013-1433-y

    Article  Google Scholar 

  • Xie L, Hongmei C, Yang J (2013) Conidia production by Beauveria bassiana on rice in solid-state fermentation using tray bioreactor. Adv Mat Res 610–613:3478–3482. doi:10.4028/www.scientific.net/AMR.610-613.3478

    Article  Google Scholar 

  • Xie L, Han JH, Kim JJ, Lee SY (2016) Effects of culture conditions on conidial production of the sweet potato whitefly pathogenic fungus Isaria javanica. Mycoscience 57:64–70. doi:10.1016/j.myc.2015.09.002

    Article  Google Scholar 

  • Yanagawa A, Imai T, Akino T, Toh Y, Yoshimura T (2015) Olfactory cues from pathogenic fungus affect the direction of motion of termites, Coptotermes formosanus. J Chem Ecol 41:1118–1126. doi:10.1007/s10886-015-0649-8

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the National Council for Science and Technology (CONACyT) for the Project CB-2015-254819, and also the Universidad Autónoma Metropolitana (UAM).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Octavio Loera.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 59 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Muñiz-Paredes, F., Miranda-Hernández, F. & Loera, O. Production of conidia by entomopathogenic fungi: from inoculants to final quality tests. World J Microbiol Biotechnol 33, 57 (2017). https://doi.org/10.1007/s11274-017-2229-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-017-2229-2

Keywords

Navigation