Characterization of a Biofilm Bioreactor Designed for the Single-Step Production of Aerial Conidia and Oosporein by Beauveria bassiana PQ2
Abstract
:1. Introduction
2. Materials and Methods
2.1. Fungal Strain and Media
2.2. Biofilm Reactor Setup
2.3. Fungal Growth Evaluation, Aerial Conidia, and Red Pigment Production Dynamics
2.4. Oosporein Characterization by HPLC Tandem Mass Spectrometry
2.5. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Da Costa Souza, P.N.; Bim Grigoletto, T.L.; Beraldo de Moraes, L.A.; Abreu, L.M.; Souza Guimarães, L.H.; Santos, C.; Ribeiro Galvão, L.; Gomes Cardoso, P. Production and chemical characterization of pigments in filamentous fungi. Microbiology 2016, 162, 12–22. [Google Scholar] [CrossRef]
- Neera, D.K.; Ramana, K.V.; Sharma, R.K. Optimization of Monascus pigment production and its antibacterial activity. Int. J. Curr. Res. Biosci. Plant Biol. 2017, 4, 71–80. [Google Scholar] [CrossRef] [Green Version]
- Barra-Bucarei, L.; González, M.G.; Iglesias, A.F.; Aguayo, G.S.; Peñalosa, M.G.; Vera, P.V. Beauveria bassiana multifunction as an endophyte: Growth promotion and biologic control of Trialeurodes vaporariorum, (Westwood) (Hemiptera: Aleyrodidae) in tomato. Insects 2020, 11, 591. [Google Scholar] [CrossRef]
- Stracquadanio, C.; Quiles, J.M.; Meca, G.; Cacciola, S.O. Antifungal activity of bioactive metabolites produced by Trichoderma asperellum and Trichoderma atroviride in liquid medium. J. Fungi 2020, 6, 263. [Google Scholar] [CrossRef]
- Soesanto, L.; Sari, L.Y.; Mugiastuti, E.; Manan, A. Cross application of entomopathogenic fungi raw secondary metabolites for controlling fusarium wilt of chili seedlings. Jurnal Hama Penyakit Tumbuhan Tropika 2021, 21, 82–90. [Google Scholar] [CrossRef]
- Manan, M.; Webb, C. Design aspects of solid state fermentation as applied to microbial bioprocessing. J. Appl. Biotechnol. Bioeng. 2017, 4, 91. [Google Scholar] [CrossRef] [Green Version]
- Hussain, A.; Tian, M.-Y.; Ahmed, S.; Shahid, M. Current status of entomopathogenic fungi as mycoinecticides and their inexpensive development in liquid cultures. In Zoologia; García, M.D., Ed.; InTech: Rijeka, Croatia, 2012; pp. 103–122. [Google Scholar]
- Pradeep, F.S.; Begam, M.S.; Palaniswamy, M.; Pradeep, B. Influence of culture media on growth and pigment production by Fusarium moniliforme KUMBF1201 isolated from paddy field soil. World Appl. Sci. J. 2013, 22, 70–77. [Google Scholar] [CrossRef]
- Cruz Barrera, M.; Gómez, M.I.; Serrato Bermúdez, J.C. Towards the production of fungal biocontrol candidates using inert supports: A case of study of Trichoderma asperellum in a pilot fixed bed fermenter. Biocontrol Sci. Technol. 2019, 29, 162–184. [Google Scholar] [CrossRef]
- Méndez-González, F.; Loera-Corral, O.; Saucedo-Castañeda, G.; Favela-Torres, E. Bioreactors for the production of biological control agents produced by solid-state fermentation. In Current Developments in Biotechnology and Bioengineering; Pandey, A., Larroche, C., Soccol, C.R., Eds.; Elsevier: Amsterdam, The Netherlands, 2018; pp. 109–121. [Google Scholar]
- Lohse, R.; Jakobs-Schönwandt, D.; Vidal, S.; Patel, A.V. Evaluation of new fermentation and formulation strategies for a high endophytic establishment of Beauveria bassiana in oilseed rape plants. Biological. Control 2015, 88, 26–36. [Google Scholar] [CrossRef]
- Valencia, J.W.A.; Gaitán Bustamante, A.L.; Jiménez, A.V.; Grossi-de-Sá, M.F. Cytotoxic activity of fungal metabolites from the pathogenic fungus Beauveria bassiana: An intraspecific evaluation of beauvericin production. Curr. Microbiol. 2011, 63, 306. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mao, B.-Z.; Huang, C.; Yang, G.-M.; Chen, Y.-Z.; Chen, S.-Y. Separation and determination of the bioactivity of oosporein from Chaetomium cupreum. Afr. J. Biotechnol. 2010, 9. [Google Scholar] [CrossRef]
- Mwamburi, L.A.; Laing, M.D.; Miller, R.M. Laboratory screening of insecticidal activities of Beauveria bassiana and Paecilomyces lilacinus against larval and adult house fly (Musca domestica L.): Research article. Afr. Entomol. 2010, 18, 38–46. [Google Scholar] [CrossRef]
- Feng, P.; Shang, Y.; Cen, K.; Wang, C. Fungal biosynthesis of the bibenzoquinone oosporein to evade insect immunity. Proc. Natl. Acad. Sci. USA 2015, 112, 11365. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Alurappa, R.; Bojegowda, M.R.M.; Kumar, V.; Mallesh, N.K.; Chowdappa, S. Characterisation and bioactivity of oosporein produced by endophytic fungus Cochliobolus kusanoi isolated from Nerium oleander L. Nat. Prod. Res. 2014, 28, 2217–2220. [Google Scholar] [CrossRef]
- Nagaoka, T.; Nakata, K.; Kouno, K. Antifungal activity of oosporein from an antagonistic fungus against Phytophthora infestans. Z. Nat. C 2004, 59, 302–304. [Google Scholar] [CrossRef] [Green Version]
- Ramesha, A.; Venkataramana, M.; Nirmaladevi, D.; Gupta, V.K.; Chandranayaka, S.; Srinivas, C. Cytotoxic effects of oosporein isolated from endophytic fungus Cochliobolus kusanoi. Front. Microbiol. 2015, 6, 870. [Google Scholar] [CrossRef]
- Koch, E.; Ole Becker, J.; Berg, G.; Hauschild, R.; Jehle, J.; Köhl, J.; Smalla, K. Biocontrol of plant diseases is not an unsafe technology! J. Plant Dis. Prot. 2018, 125, 121–125. [Google Scholar] [CrossRef]
- Khalesi, M.; Zune, Q.; Telek, S.; Riveros-Galan, D.; Verachtert, H.; Toye, D.; Gebruers, K.; Derdelinckx, G.; Delvigne, F. Fungal biofilm reactor improves the productivity of hydrophobin HFBII. Biochem. Eng. J. 2014, 88, 171–178. [Google Scholar] [CrossRef]
- Musoni, M.; Destain, J.; Thonart, P.; Bahama, J.-B.; Delvigne, F. Bioreactor design and implementation strategies for the cultivation of filamentous fungi and the production of fungal metabolites: From traditional methods to engineered systems. Biotechnol. Agron. Soc. Environ. 2015, 19, 430–442. [Google Scholar]
- Moutafchieva, D.; Popova, D.; Dimitrova, M.; Tchaoushev, S. Experimental determination of the volumetric mass transfer coefficient. J. Chem. Technol. Metall. 2013, 48, 351–356. [Google Scholar]
- Aguilar-Zárate, P.; Wong-Paz, J.E.; Rodríguez-Duran, L.V.; Buenrostro-Figueroa, J.; Michel, M.; Saucedo-Castañeda, G.; Favela-Torres, E.; Ascacio-Valdés, J.A.; Contreras-Esquivel, J.C.; Aguilar, C.N. On-line monitoring of Aspergillus niger GH1 growth in a bioprocess for the production of ellagic acid and ellagitannase by solid-state fermentation. Bioresour. Technol. 2018, 247, 412–418. [Google Scholar] [CrossRef] [PubMed]
- Cooper, C.; Fernstrom, G.; Miller, S. Performance of agitated gas-liquid contactors. Ind. Eng. Chem. 1944, 36, 504–509. [Google Scholar] [CrossRef]
- Garcia-Ochoa, F.; Gomez, E. Bioreactor scale-up and oxygen transfer rate in microbial processes: An overview. Biotechnol. Adv. 2009, 27, 153–176. [Google Scholar] [CrossRef]
- De la Cruz-Quiroz, R.; Roussos, S.; Aguilar, C.N. Production of a biological control agent: Effect of a drying process of solid-state fermentation on viability of Trichoderma spores. Int. J. Green Tech. 2018, 4, 1–6. [Google Scholar]
- Aguilar-Zarate, P.; Cruz-Hernandez, M.A.; Montañez, J.C.; Belmares-Cerda, R.E.; Aguilar, C.N. Enhancement of tannase production by Lactobacillus plantarum CIR1: Validation in gas-lift bioreactor. Bioprocess Biosyst. Eng. 2014, 37, 2305–2316. [Google Scholar] [CrossRef] [PubMed]
- Seye, F.; Bawin, T.; Boukraa, S.; Zimmer, J.-Y.; Ndiaye, M.; Delvigne, F.; Francis, F. Pathogenicity of Aspergillus clavatus produced in a fungal biofilm bioreactor toward Culex quinquefasciatus (Diptera: Culicidae). J. Pestic. Sci. 2014, 39, 127–132. [Google Scholar] [CrossRef] [Green Version]
- Zune, Q.; Delepierre, A.; Gofflot, S.; Bauwens, J.; Twizere, J.C.; Punt, P.J.; Francis, F.; Toye, D.; Bawin, T.; Delvigne, F. A fungal biofilm reactor based on metal structured packing improves the quality of a Gla::GFP fusion protein produced by Aspergillus oryzae. Appl. Microbiol. Biotechnol. 2015, 99, 6241–6254. [Google Scholar] [CrossRef] [Green Version]
- Kang, S.W.; Lee, S.H.; Yoon, C.S.; Kim, S.W. Conidia production by Beauveria bassiana (for the biocontrol of a diamondback moth) during solid-state fermentation in a packed-bed bioreactor. Biotechnol. Lett. 2005, 27, 135. [Google Scholar] [CrossRef] [PubMed]
- Pham, T.A.; Kim, J.J.; Kim, K. Optimization of solid-state fermentation for improved conidia production of Beauveria bassiana as a mycoinsecticide. Mycobiology 2010, 38, 137–143. [Google Scholar] [CrossRef] [Green Version]
- Mascarin, G.M.; Jackson, M.A.; Kobori, N.N.; Behle, R.W.; Dunlap, C.A.; Delalibera Júnior, Í. Glucose concentration alters dissolved oxygen levels in liquid cultures of Beauveria bassiana and affects formation and bioefficacy of blastospores. Appl. Microbiol. Biotechnol. 2015, 99, 6653–6665. [Google Scholar] [CrossRef] [PubMed]
- Santa, H.S.D.; Santa, O.R.D.; Brand, D.; Vandenberghe, L.P.d.S.; Soccol, C.R. Spore production of Beauveria bassiana from agro-industrial residues. Braz. Arch. Biol. Technol. 2005, 48, 51–60. [Google Scholar] [CrossRef] [Green Version]
- Damiani, A.L.; Kim, M.H.; Wang, J. An improved dynamic method to measure kLa in bioreactors. Biotechnol. Bioeng. 2014, 111, 2120–2125. [Google Scholar] [CrossRef] [PubMed]
- Nogueira, R.; Lazarova, V.; Manem, J.; Melo, L.F. Influence of dissolved oxygen on the nitrification kinetics in a circulating bed biofilm reactor. Bioprocess Eng. 1998, 19, 441–449. [Google Scholar] [CrossRef] [Green Version]
- Pérez, J.; Montesinos, J.L.; Gòdia, F. Gas–liquid mass transfer in an up-flow cocurrent packed-bed biofilm reactor. Biochem. Eng. J. 2006, 31, 188–196. [Google Scholar] [CrossRef]
- García-Gutiérrez, C.; González-Maldonado, M.B.; Medrano-Roldán, H.; Solís-Soto, A. Study of the mixing conditions in bioreactor for blastospores production of Beauveria bassiana. Rev. Colombiana Biotecnol. 2013, 15, 47–54. [Google Scholar]
- Kurt, T.; Marbà-Ardébol, A.-M.; Turan, Z.; Neubauer, P.; Junne, S.; Meyer, V. Rocking Aspergillus: Morphology-controlled cultivation of Aspergillus niger in a wave-mixed bioreactor for the production of secondary metabolites. Microbial. Cell Factories 2018, 17, 128. [Google Scholar] [CrossRef] [Green Version]
- Pavlík, M.; Fleischer, P.; Fleischer, P.; Pavlík, M.; Šuleková, M. Evaluation of the carbon dioxide production by fungi under different growing conditions. Curr. Microbiol. 2020, 77, 2374–2384. [Google Scholar] [CrossRef]
- Da Cunha, L.P.; Casciatori, F.P.; Vicente, I.V.; Garcia, R.L.; Thoméo, J.C. Metarhizium anisopliae conidia production in packed-bed bioreactor using rice as substrate in successive cultivations. Process Biochem. 2020, 97, 104–111. [Google Scholar] [CrossRef]
- Song, M.H.; Yu, J.S.; Kim, S.; Lee, S.J.; Kim, J.C.; Nai, Y.-S.; Shin, T.Y.; Kim, J.S. Downstream processing of Beauveria bassiana and Metarhizium anisopliae-based fungal biopesticides against Riptortus pedestris: Solid culture and delivery of conidia. Biocontrol Sci. Technol. 2019, 29, 514–532. [Google Scholar] [CrossRef]
- Sala, A.; Artola, A.; Sánchez, A.; Barrena, R. Rice husk as a source for fungal biopesticide production by solid-state fermentation using B. bassiana and T. harzianum. Bioresour. Technol. 2020, 296, 122322. [Google Scholar] [CrossRef]
- Ávila-Hernández, J.; Carrillo-Inungaray, M.; De-La-Cruz-Quiroz, R.; Wong-Paz, J.; Muñiz-Márquez, D.; Parra, R.; Aguilar, C.; Aguilar-Zárate, P. Beauveria bassiana secondary metabolites: A review inside their production systems, biosynthesis, and bioactivities. Mex. J. Biotechnol. 2020, 5, 1–33. [Google Scholar] [CrossRef]
- Strasser, H.; Abendstein, D.; Stuppner, H.; Butt, T.M. Monitoring the distribution of secondary metabolites produced by the entomogenous fungus Beauveria brongniartii with particular reference to oosporein. Mycol. Res. 2000, 104, 1227–1233. [Google Scholar] [CrossRef]
- Amin, G.A.; Youssef, N.A.; Bazaid, S.; Saleh, W.D. Assessment of insecticidal activity of red pigment produced by the fungus Beauveria bassiana. World J. Microbiol. Biotechnol. 2010, 26, 2263–2268. [Google Scholar] [CrossRef]
- Ng, H.E.; Raj, S.S.A.; Wong, S.H.; Tey, D.; Tan, H.M. Estimation of fungal growth using the ergosterol assay: A rapid tool in assessing the microbiological status of grains and feeds. Lett. Appl. Microbiol. 2008, 46, 113–118. [Google Scholar] [CrossRef]
Flow Rate (L/min) | KLa Liquid Phase (min−1) | KLa Gaseous Phase (min−1) |
---|---|---|
1.5 | 0.99 ± 0.009 b | 0.51 ± 0.261 b |
2.0 | 1.16 ± 0.017 b | 0.58 ± 0.102 b |
2.5 | 2.10 ± 0.017 a | 3.66 ± 0.394 a |
Parameters | Units | Value |
---|---|---|
CO2 max | mg CO2 mL−1 | 80.59 |
µ | h−1 | 0.04 |
Growth model | R2 | 0.99 |
Oosporeinmax | mgL−1 | 183.0 |
Oosporein productivity | mg/L/h | 1.09 |
Oosporein model | R2 | 0.97 |
YOosp/CO2 | mg Oosporein/h × mg CO2 | 0.02 |
Conidia recovery | Conidia/gram of support | 1.24 × 109 |
Peak No. | R. T. (min) | M. W. | [M-H] − (m/z) | MS2 Ion Fragment | Tentative Identity |
---|---|---|---|---|---|
1 | 3.40 | 283 | 282 | 150, 133 | Unknown |
2 | 5.92 | 244 | 243 | 200, 110 | Unknown |
3 | 12.84 | 291 | 290 | 254, 230, 214, 200, 128 | Unknown |
4 | 15.49 | 387 | 386 | 343, 299, 298, 286 | Unknown |
5 | 22.72 | 306 | 305 | 277, 262, 261, 249, 233, 217, 205, 189, 161 | Oosporein |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Lara-Juache, H.R.; Ávila-Hernández, J.G.; Rodríguez-Durán, L.V.; Michel, M.R.; Wong-Paz, J.E.; Muñiz-Márquez, D.B.; Veana, F.; Aguilar-Zárate, M.; Ascacio-Valdés, J.A.; Aguilar-Zárate, P. Characterization of a Biofilm Bioreactor Designed for the Single-Step Production of Aerial Conidia and Oosporein by Beauveria bassiana PQ2. J. Fungi 2021, 7, 582. https://doi.org/10.3390/jof7080582
Lara-Juache HR, Ávila-Hernández JG, Rodríguez-Durán LV, Michel MR, Wong-Paz JE, Muñiz-Márquez DB, Veana F, Aguilar-Zárate M, Ascacio-Valdés JA, Aguilar-Zárate P. Characterization of a Biofilm Bioreactor Designed for the Single-Step Production of Aerial Conidia and Oosporein by Beauveria bassiana PQ2. Journal of Fungi. 2021; 7(8):582. https://doi.org/10.3390/jof7080582
Chicago/Turabian StyleLara-Juache, Héctor Raziel, José Guadalupe Ávila-Hernández, Luis Víctor Rodríguez-Durán, Mariela Ramona Michel, Jorge Enrique Wong-Paz, Diana Beatriz Muñiz-Márquez, Fabiola Veana, Mayra Aguilar-Zárate, Juan Alberto Ascacio-Valdés, and Pedro Aguilar-Zárate. 2021. "Characterization of a Biofilm Bioreactor Designed for the Single-Step Production of Aerial Conidia and Oosporein by Beauveria bassiana PQ2" Journal of Fungi 7, no. 8: 582. https://doi.org/10.3390/jof7080582