Abstract
To determine the growth kinetic parameters, substrate consumption and spore yields for Bacillus thuringiensis, liquid fermentation (SmF) and solid-state fermentation (SSF), on polyurethane foam (PUF), were analysed comprising strictly the same media. The analysis included three medium concentrations, maintaining the same C/N ratio, with initial glucose at 12.5, 25, and 50 g L−1 (1X, 2X and 4X, respectively). SSF at 2X and 4X produced higher amounts of total biomass, vegetative growth and even early sporulation. Notably, at all glucose concentrations, sporulation was not inhibited in SSF as seen partially in SmF at 2X, and totally at 4X. Micrographs from PUF cultures showed thin layers of bacteria forming large horizontal aggregates, associated with the higher biomass yields and the early cell differentiation. This is the first work showing that SSF improves spore yields of B. thuringiensis in media with high substrate concentrations, using PUF as a research tool for comparative analysis with application in new production systems including biofilm-forming microorganisms.
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Glare T, Caradus J, Gelernter W, Jackson T, Keyhani N, Köhl J, Marrone P, Morin L, Stewart A (2012) Have biopesticides come of age? Trends Biotechnol. https://doi.org/10.1016/j.tibtech.2012.01.003
Wang J, Mei H, Qian H, Tang Q, Liu X, Yu Z, He J (2013) Expression profile and regulation of spore and parasporal crystal formation-associated genes in Bacillus thuringiensis. J Proteome Res 15:6. https://doi.org/10.1021/pr4003728
Mounsef JR, Salameh D, Louka N, Brandam C, Lteif R (2015) The effect of aeration conditions, characterized by the volumetric mass transfer coefficient KLa, on the fermentation kinetics of Bacillus thuringiensis kurstaki. J Biotechnol. https://doi.org/10.1016/j.jbiotec.2015.06.387
Navarro-Martinez AK, Pérez-Guevara F (2014) Construction of a biodynamic model for cry protein production studies. AMB Express. https://doi.org/10.1186/s13568-014-0079-y
Sarrafzadeh MH, Schorr-Galindo S, La HJ, Oh HM (2014) Aeration effects on metabolic events during sporulation of Bacillus thuringiensis. J Microbiol. https://doi.org/10.1007/s12275-014-3547-9
Slamti L, Perchat S, Huillet E, Lereclus D (2014) Quorum sensing in Bacillus thuringiensis is required for completion of a full infectious cycle in the insect. Toxins (Basel). https://doi.org/10.3390/toxins6082239
Verplaetse E, Slamti L, Gohar M, Lereclus D (2015) Cell differentiation in a Bacillus thuringiensis population during planktonic growth, biofilm formation, and host infection. MBio. https://doi.org/10.1016/j.resmic.2016.03.006
Verplaetse E, Slamti L, Gohar M, Lereclus D (2017) Two distinct pathways lead Bacillus thuringiensis to commit to sporulation in biofilm. Res Microbiol. https://doi.org/10.1016/j.resmic.2016.03.006
Mols M, Abee T (2011) Primary and secondary oxidative stress in Bacillus. Environ Microbiol. https://doi.org/10.1111/j.1462-2920.2011.02433.x
López-Pérez M, Viniegra-González G (2016) Production of protein and metabolites by yeast grown in solid state fermentation: present status and perspectives. J Chem Technol Biotechnol. https://doi.org/10.1002/jctb.4819
Soccol CR, da Costa ES, Letti LA, Karp SG, Woiciechowski LP, Vandenberghe LP (2017) Recent developments and innovations in solid state fermentation. Biotechnol Res Innov. https://doi.org/10.1016/j.biori.2017.01.002
Hayrapetyan H, Abee T, Nierop Groot M (2016) Sporulation dynamics and spore heat resistance in wet and dry biofilms of Bacillus cereus. Food Control. https://doi.org/10.1016/j.foodcont.2015.08.027
van der Voort M, Abee T (2013) Sporulation environment of emetic toxin-producing Bacillus cereus strains determines spore size, heat resistance and germination capacity. J Appl Microbiol. https://doi.org/10.1111/jam.12118
Jisha VN, Babysarojam Smitha R, Priji P, Sajith S, Benjamin S (2014) Biphasic fermentation is an efficient strategy for the overproduction of δ-endotoxin from Bacillus thuringiensis. Appl Biochem Biotechnol. https://doi.org/10.1007/s12010-014-1383-3
Narayanan JV, Babysarojam SR, Faisal PA, Niravath R, Moolath BG (2017) Crude Bacillus thuringiensis pellets efficiently combats Eutetranychus orientalis, the spider mite. Int J Pest Manag. https://doi.org/10.1080/09670874.2017.1390622
Sailas B (2015) Bacillus thuringiensis subsp. kurstaki in raw solid fermented matter efficiently combats the coconut pest. Aceria guerreronis Keifer Bt Res 15:8. https://doi.org/10.5376/bt.2015.06.0002
Smitha RB, Jisha VN, Sajith S, Benjamin S (2013) Dual production of amylase and δ-endotoxin by Bacillus thuringiensis subsp. kurstaki during biphasic fermentation. Microbiology. https://doi.org/10.1134/S0026261714010147
Dinorín-Téllez-Girón J, Delgado-Macuil RJ, Larralde Corona CP, Martínez Montes FJ, de la Torre Martínez M, López-Y-López VE (2015) Reactance and resistance: main properties to follow the cell differentiation process in Bacillus thuringiensis by dielectric spectroscopy in real time. Appl Microbiol Biotechnol. https://doi.org/10.1007/s00253-015-6562-9
Lima-Pérez J, Rodríguez-Gómez D, Loera O, Viniegra-González G, López-Pérez M (2018) Differences in growth physiology and aggregation of Pichia pastoris cells between solid state and submerged fermentations under aerobic conditions. J Chem Technol Biotechnol. https://doi.org/10.1002/jctb.5384
Xiao Z, Storms R, Tsang A (2005) Microplate-based carboxymethylcellulose assay for endoglucanase activity. Anal Biochem. https://doi.org/10.1016/j.ab.2005.01.052
Gatto M, Muratori S, Rinaldi S (1988) A functional interpretation of the logistic equation. Ecol Modell. https://doi.org/10.1016/0304-3800(88)90113-5
Pirt SJ (1975) Principles of microbe and cell cultivation. Blackwell Scientific Publications, Oxford
Berbert-Molina MA, Prata MR, Pessanha LG, Silveira MM (2008) Kinetics of Bacillus thuringiensis var. israelensis growth on high glucose concentrations. J Ind Microbiol Biotechnol. https://doi.org/10.1007/s10295-008-0439-1
Viniegra-González G, Favela-Torres E, Aguilar CN, de Rómero-Gomez SJ, Díaz-Godínez G, Augur C (2003) Advantages of fungal enzyme production in solid state over liquid fermentation systems. Biochem Eng J. https://doi.org/10.1016/S1369-703X(02)00128-6
Boniolo FS, Rodrigues RC, Prata AMR, López ML, Jacinto T, Da Silveira MM, Berbert-Molina MA (2012) Oxygen supply in Bacillus thuringiensis fermentations: bringing new insights on their impact on sporulation and δ-endotoxin production. Appl Microbiol Biotechnol. https://doi.org/10.1007/s00253-011-3746-9
Asaff A, Cerda-García-Rojas CM, Viniegra-González G, de la Torre M (2006) Carbon distribution and redirection of metabolism in Paecilomyces fumosoroseus during solid state and liquid fermentations. Process Biochem. https://doi.org/10.1016/j.procbio.2006.01.001
Battino R (1981) Oxygen and ozone (Data Series). Pergamon Press, Ohio, p 519
Rischbieter E, Schumpe A, Wunder V (1996) Gas solubilities in aqueous solutions of organic substances. J Chem Eng Data 41:809–812. https://doi.org/10.1021/je960039c
Devidas PC, Pandit BH, Vitthalrao PS (2014) Evaluation of different culture media for improvement in bioinsecticides production by indigenous Bacillus thuringiensis and their application against larvae of Aedes aegypti. Sci World J. https://doi.org/10.1155/2014/273030
Zouari N, Achour O, Jaoua S (2002) Production of delta-endotoxin by Bacillus thuringiensis subsp kurstaki and overcoming of catabolite repression by using highly concentrated gruel and fish meal media in 2 and 20 dm3 fermenters. J Chem Technol Biotechnol. https://doi.org/10.1002/jctb.650
López-Pérez 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. https://doi.org/10.1002/jctb.2306
Čáp M, Váchová L, Palková Z (2012) Reactive oxygen species in the signaling and adaptation of multicellular microbial communities. Oxid Med Cell Longev. https://doi.org/10.1155/2012/976753
Frey RL, He L, Cui Y, Decho AW, Kawaguchi T, Ferguson PL, Ferry JL (2010) Reaction of N-acylhomoserine lactones with hydroxyl radicals: rates, products, and effects on signaling activity. Environ Sci Technol. https://doi.org/10.1021/es100663e
Green J, Rolfe MD, Smith LJ (2014) Transcriptional regulation of bacterial virulence gene expression by molecular oxygen and nitric oxide. Virulence. https://doi.org/10.4161/viru.27794
Hall PR, Elmore BO, Spang CH, Alexander SM, Manifold-Wheeler BC, Castleman MJ, Daly SM, Peterson MM, Sully EK, Femling JK, Otto M, Horswill AR, Timmins GS, Gresham HD (2013) Nox2 modification of LDL is essential for optimal apolipoprotein B-mediated control of agr Type III Staphylococcus aureus quorum-sensing. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1003166
Yarwood JM, Paquette KM, Tikh UB, Volper EM, Greenberg EP (2007) Generation of virulence factor variants in Staphylococcus aureus biofilms. J Bacteriol. https://doi.org/10.1128/JB.00789-07
Kim HY, Heo DY, Park HM, Singh D, Lee CH (2016) Metabolomic and transcriptomic comparison of solid state and submerged fermentation of Penicillium expansum KACC 40815. PLoS One. https://doi.org/10.1371/journal.pone.0149012
Pérez-Guzmán D, Montesinos-Matías R, Arce-Cervantes O, Gómez-Quiroz LE, Loera O, Garza-López PM (2016) Reactive oxygen species production, induced by atmospheric modification, alter conidial quality of Beauveria bassiana. J Appl Microbiol. https://doi.org/10.1111/jam.13156
Chen D, Xu D, Li M, He J, Gong Y, Wu D, Sun M, Yu Z (2012) Proteomic analysis of Bacillus thuringiensis δphaC mutant BMB171/PHB-1 reveals that the PHB synthetic pathway warrants normal carbon metabolism. J Proteom. https://doi.org/10.1016/j.jprot.2012.06.002
Jing-Wen Z, Ya-Fei C, Zheng-Hong X, Zi-Niu Y, Shou-Wen C (2007) Production of thuringiensin by fed-batch culture of Bacillus thuringiensis subsp. darmstadiensis 032 with an improved pH-control glucose feeding strategy. Process Biochem. https://doi.org/10.1016/j.procbio.2006.07.017
Liu X, Zuo M, Wang T, Sun Y, Liu S, Hu S, He H, Yang Q, Rang J, Quan M, Xia L, Ding X (2015) Proteomic analysis of the influence of Cu2+ on the crystal protein production of Bacillus thuringiensis X022. Cell Fact, Microb. https://doi.org/10.1186/s12934-015-0339-9
Kraemer-Schafhalter A, Moser A (1996) Kinetic study of Bacillus thuringiensis var. israelensis in lab-scale batch process. Bioprocess Eng 14:139–144
Acknowledgements
We are grateful for financial support of the Universidad Autónoma Metropolitana for this research. We also thank the Consejo Nacional de Ciencia y Tecnología (CONACYT) for the fellowship granted to J. Lima-Pérez.
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Lima-Pérez, J., López-Pérez, M., Viniegra-González, G. et al. Solid-state fermentation of Bacillus thuringiensis var kurstaki HD-73 maintains higher biomass and spore yields as compared to submerged fermentation using the same media. Bioprocess Biosyst Eng 42, 1527–1535 (2019). https://doi.org/10.1007/s00449-019-02150-5
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DOI: https://doi.org/10.1007/s00449-019-02150-5