Bacillus based microbial formulations: Optimization of the production process

Main Article Content

Sandra Stamenković Stojanović
https://orcid.org/0000-0001-6706-9318
Ivana Karabegović
https://orcid.org/0000-0003-2191-4082
Vladimir Beškoski
https://orcid.org/0000-0002-6372-4706
Nada Nikolić
Miodrag Lazić

Abstract

Bacillus sp.-based microbial formulations have found wide application in many fields: from pharmacy and medicine to environmental protection and agriculture due to the ability of this species to produce various metabolites and to form endospores. Recently, these products have gained popularity as biopesticidal and phytostimulatory agents, which are a "green" alternative to overused agrochemicals. In order to obtain a high-quality and long-lasting product with desired characteristics, it is necessary to optimize the production process at each stage, which implies coordinating the microbial species, the type and the conditions of microbial cultivation along with formulation technologies. This paper provides a concise overview of the most important findings in this area, regarding characteristics of microbial formulations and specific criteria that need to be met when such a product is formulated. It should serve as a beginning point for everyone starting new research, not just in the field of biofertilization and biological control of plant diseases, but generally in the field of biochemical engineering.

Downloads

Download data is not yet available.

Article Details

How to Cite
Stamenković Stojanović, S., Karabegović, I., Beškoski, V., Nikolić, N., & Lazić, M. (2019). Bacillus based microbial formulations: Optimization of the production process. HEMIJSKA INDUSTRIJA (Chemical Industry), 73(3), 169–182. https://doi.org/10.2298/HEMIND190214014S
Section
Biochemical Engineering - General
Author Biographies

Sandra Stamenković Stojanović, University of Niš, Faculty of Technology, Bulevar Oslobođenja 124, 16000 Leskovac

Department for food technology and Biotechnology

PhD student

Teaching assistant 

Ivana Karabegović, University of Niš, Faculty of Technology, Bulevar Oslobođenja 124, 16000 Leskovac

Department for Food technology and Biotechnology 

 Assistant professor 

Vladimir Beškoski, University of Belgrade, Faculty of Chemistry, Studentski trg 12-16, 11000 Belgrade

Department for biochemistry

Nada Nikolić, University of Niš, Faculty of Technology, Bulevar Oslobođenja 124, 16000 Leskovac

Department for Food technology and Biotechnology 

 Full professor 

Miodrag Lazić, University of Niš, Faculty of Technology, Bulevar Oslobođenja 124, 16000 Leskovac

Department for Food technology and Biotechnology 

 Full professor 

References

Shahcheraghi S, Ayatollahi J, Lotfi M. Applications of Bacillus subtilis as an important bacterium in medical sciences and human life. Trop J Med Res. 2015; 18(1): 1-9.

Mercado-Flores Y, Cárdenas-Álvarez IO, Rojas-Olvera AV, Pérez-Camarillo JP, Leyva Mir SG, Anducho-Reyes MA. Application of Bacillus subtilis in the biological control of 359 the phytopathogenic fungus Sporisoriumreilianum. Biol Control. 2014; 76: 36-40.

Schallmey M, Singh A, Ward OP. Developments in the use of Bacillus species for industrial production. Can J Microbiol. 2004;50(1):1-17.

Govedarica M, Nada M, Mirjana J, Simonida Đ, Zora J, Janja K, Snežana Đ. Primenabiofertilizera, biostimulatora i biopesticida u poljoprivrednoj proizvodnji. Naučni Inst za Ratar i Povrt Novi Sad, ZbornikRadova 2002; 37: 85-95. (in Serbian)

Benhamou N, Kloepper JW, Tuzun S. Induction of resistance against Fusarium wilt of tomato by combination of chitosan with an endophytic bacterial strain: Ultrastructure and cytochemistry of the host response. Planta. 1998;204(2):153-168.

Wei Z, Yang X, Yin S, Shen Q, Ran W, Xu Y. Efficacy of Bacillus-fortified organic fertiliser in controlling bacterial wilt of tomato in the field. Appl Soil Ecol. 2011;48(2):152-159.

Yazdani M, Bahmanyar MA, Pirdashti H, Ali M. Effect of Phosphate Solubilization Microorganisms (PSM) and Plant Growth Promoting Rhizobacteria ( PGPR ) on Yield and Yield Components of Corn ( Zea mays L .). World Acad Sci Eng Technol. 2009;25(1):90-92.

Iqbal Hossain M, Sadekuzzaman M, Ha S-D. Probiotics as potential alternative biocontrol agents in the agriculture and food industries: A review. Food Res Int. 2017;100:63-73.

de Carvalho ALU, de Oliveira FHPC, Mariano R de LR, Gouveia ER, Souto-Maior AM. Growth, sporulation and production of bioactive compounds by Bacillus subtilis R14. Brazilian Arch Biol Technol. 2010;53(3):643-652.

Martinez-Alvarez JC, Castro-Martinez C, Sanchez-Pena P, Gutierrez-Dorado R, Maldonado-Mendoza IE. Development of a powder formulation based on Bacillus cereussensulato strain B25 spores for biological control of Fusarium verticillioides in maize plants. World J Microbiol Biotechnol. 2016;32(5):1-10.

Wang S., Zhong JJ. Bioreactor engineering. In: Yang ST, ed. Bioprocessing for Value-Added Products from Renewable Resources. Amsterdam: Elsevier; 2007.

Najafpour GD. Biochemical Engineering and Biotechnology. Amsterdam: Elsevier; 2007.

Doran PM. Bioprocess Engineering Principles: Second Edition. London: Academic Press; 2013.

Chumthong A, Kanjanamaneesathian M, Pengnoo A, Wiwattanapatapee R. Water-soluble granules containing Bacillus megaterium for biological control of rice sheath blight: Formulation, bacterial viability and efficacy testing. World J Microbiol Biotechnol. 2008;24:2499.

Cho J-H, Kim Y-B, Kim E-K. Optimization of culture media for Bacillus species by statistical experimental design methods. Korean J Chem Eng. 2009;26(3):754-759.

Posada-Uribe LF, Romero-Tabarez M, Villegas-Escobar V. Effect of medium components and culture conditions in Bacillus subtilis EA-CB0575 spore production. Bioprocess Biosyst Eng. 2015;38(10):1879-1888.

Bjelić D. Karakterizacija i efektivnost bakterija promotora biljnograsta izolovanih iz rizosfere kukuruza. Doctoral dissertation, Univerzitet u NovomSadu, Poljoprivredni 395 fakultet. 2014. (in Serbian)

Garcia-Fraile P, Menendez E, Rivas R. Role of bacterial biofertilizers in agriculture and forestry. AIMS Bioeng. 2015;2(3):183-205.

Abhilash PC, Dubey RK, Tripathi V, Gupta VK, Singh HB. Plant Growth-Promoting Microorganisms for Environmental Sustainability. Trends Biotechnol. 2016;xx:1-4.

Owen D, Williams AP, Griffith GW, Withers PJA. Use of commercial bio-inoculants to increase agricultural production through improved phosphrous acquisition. Appl Soil Ecol. 2015;86:41-54.

Cerozi B da S, Fitzsimmons K. Use of Bacillus spp. to enhance phosphorus availability and serve as a plant growth promoter in aquaponics systems. Sci Hortic (Amsterdam). 2016;211:277-282.

Fira D, Dimkić I, Berić T, Lozo J, Stanković S. Biological control of plant pathogens by Bacillus species. J Biotechnol. 2018;285:44-55.

Hashem A, Tabassum B, Fathi Abd E. Bacillus subtilis: A plant-growth promoting rhizobacterium that also impacts biotic stress. Saudi J Biol Sci. 2019 (article in press)

Milić J, Beškoski V, Ilić M, Ali S, Gojgić-Cvijović G, Vrvić M. Bioremediation of soil heavily contaminated with crude oil and its products: Composition of the microbial consortium. J Serbian Chem Soc. 2009;74(4):455-460.

Beškoski VP, Gojgić-Cvijović GĐ, Milić JS, Ilić MV, Miletić SB, Jovančević BS, Vrvić MM. Bioremedijacija zemljišta kontaminiranog naftom i naftnim derivatima: mikroorganizmi, putanje razgradnje, tehnologije. Hem Ind. 2012; 66(2): 275-289. (in Serbian)

Beškoski VP, Gojgić-Cvijović G, Milić J, Ilić M, Miletić S, Šolević T, Vrvić MM. Ex situ bioremediation of a soil contaminated by mazut (heavy residual fuel oil) – A field experiment. Chemosphere. 2011;83(1):34-40.

Gojgić-Cvijović GD, Milić JS, Šolevic TM, Beškoski VP, Ilić M V., Djokić LS, Narančić TM, 414 Vrvić MM. Biodegradation of petroleum sludge and petroleum polluted soil by a bacterial consortium: A laboratory study. Biodegradation. 2012;23(1):1-14.

Mosquera S, González-Jaramillo LM, Orduz S, Villegas-Escobar V. Multiple response optimization of Bacillus subtilis EA-CB0015 culture and identification of antifungal metabolites. Biocatal Agric Biotechnol. 2014;3(4):378-385.

Guez JS, Chenikher S, Cassar JP, Jacques P. Setting up and modelling of overflowing fed-batch cultures of Bacillus subtilis for the production and continuous removal of lipopeptides. J Biotechnol. 2007;131(1):67-75.

Goswami M, Deka S. Biosurfactant production by a rhizosphere bacteria Bacillus altitudinisMS16 and its promising emulsification and antifungal activity. Colloids Surfaces B Biointerfaces. 2019;178:285-296.

Sharma S, Ramesh A, Johri B. Isolation and characterization of plant growth-promoting Bacillus amyloliquefaciens strain sks_bnj_1 and its influence on rhizosphere soil properties and nutrition of soybean (Glycine max L. Merrill). J Virol Microbiol. 2013;2013(2013):1-19.

Xia Zhang Q, Zhang Y, Ling He L, Lin Ji Z, Hui Tong Y. Identification of a small antimycotic peptide produced by Bacillus amyloliquefaciens. PesticBiochem Physiol. 2018; 150: 78-82.

Banerjee A, Ghoshal AK. Biodegradation of an actual petroleum wastewater in a packed bed reactor by an immobilized biomass of Bacillus cereus. J Environ Chem Eng. 2017;5(2):1696-1702.

Jovančićević B, Antić M, Pavlović I, Vrvić M, Beškoski V, Kronimus A, Schwarzbauer J. Transformation of Petroleum Saturated Hydrocarbons during Soil Bioremediation Experiments. Water Air Soil Pollut. 2008;190(1-4):299-307.

Ramadan MMMA, Šolević Knudsen T, Antić M, Beškoski VP, Vrvić MM, Schwarzbauer J, Jovančidević B. Degradability of n-alkanes during ex situ natural bioremediation of soil contaminated by heavy residual fuel oil (mazut). J Serbian Chem Soc. 2013;78(7):1035-1043.

Abdullah R, Kiran S, Iqtedar M, Kaleem A, Saleem F, Iftikhar T, Cheema JS, Naz S, Random mutagenesis and process optimization of bacterial co-culture for hyperproduction of 1,4-α-D-glucan glucanohydrolase using submerged fermentation. Hem Ind. 2018;72(6):329-339.

Akcan N, Serin B, Uyar F. Production and Optimization Parameters of Amylases from Bacillus subtilis RSKK96 Under Solid State Fermentation. 2012;26(3):233-239.

Božić N, Ruiz J, López-Santín J, Vujčić Z. Optimization of the growth and α-amylase production of Bacillus subtilis IP 5832 in shake flask and laboratory fermenter batch cultures. J Serbian Chem Soc. 2011;76(7):965-972.

Cagri-Mehmetoglu A, Kusakli S, van de Venter M. Production of polysaccharide and surfactin by Bacillus subtilis ATCC 6633 using rehydrated whey powder as the fermentation medium. J Dairy Sci. 2012;95(7):3643-9.

Yeh MS, Wei YH, Chang JS. Bioreactor design for enhanced carrier-assisted surfactin production with Bacillus subtilis.Process Biochem. 2006;41(8):1799-1805.

Grobelak A, Napora A, Kacprzak M. Using plant growth-promoting rhizobacteria (PGPR) to improve plant growth. Ecol Eng. 2015;84:22-28.

Eswari J, Anand M, Venkateswarlu C. Optimum culture medium composition for lipopeptide production by Bacillus subtilis using response surface model-based ant colony optimization. Sadhana - Acad Proc Eng Sci. 2016;41(1):55-65.

Stein T. Bacillus subtilis antibiotics: structures, syntheses and specific functions. Mol Microbiol. 2005;56(4):845-857.

Irfan M, Mushtaq Q, Tabssum F, Shakir HA, Qazi JI. Carboxymethyl cellulase production optimization from newly isolated thermophilic Bacillus subtilis K-18 for saccharification using response surface methodology. AMB Express. 2017;7:29.

Vučetić J, Veljković VB, Vrvić MM, Lazić ML. Mikrobiološke Sinteze Polisaharida. Beograd: Naučnaknjiga Beograd; 1995. (In Serbian).

Velineni S, Brahmaprakash GP. Survival and phosphate solubilizing ability of Bacillus megaterium in liquid inoculants under high temperature and desiccation stress. J Agric Sci Technol. 2011;13(5):795-802.

Zou C, Li Z, Yu D. Bacillus megaterium strain XTBG34 promotes plant growth by producing 2-pentylfuran. J Microbiol. 2010;48(4):460-466.

Santos S, Neto IFF, Machado MD, Soares HMVM, Soares E V. Siderophore Production by Bacillus megaterium: Effect of Growth Phase and Cultural Conditions. Appl BiochemBiotechnol. 2014;172(1):549-560.

Liu M, Liu X, Cheng B Sen, Ma XL, Lyu XT, Zhao XF, Ju YL, Min Z, Fang YL. Selection and evaluation of phosphate-solubilizing bacteria from grapevine rhizospheres for use as biofertilizers. Spanish J Agric Res. 2016;14(4):e1106.

Vasiee A, Behbahani BA, Yazdi FT, Moradi S. Optimization of the production conditions of the lipase produced by Bacillus cereus from rice flour through Plackett-Burman Design (PBD) and response surface methodology (RSM). MicrobPathog. 2016;101:36-43.

Zhao J-L, Zhou L-G, Wu J-Y. Promotion of Salvia miltiorrhiza hairy root growth and tanshinone production by polysaccharide–protein fractions of plant growth-promoting rhizobacterium Bacillus cereus. Process Biochem. 2010;45(9):1517-1522.

Lizárraga-Sánchez GJ, Leyva-Madrigal KY, Sánchez-Peña P, Quiroz-Figueroa FR, Maldonado-Mendoza IE. Bacillus cereus sensulato strain B25 controls maize stalk and ear rot in Sinaloa, Mexico. F Crop Res. 2015;176:11-21.

Vidhyalakshmi R, Valli NC, Narendra Kumar G, Sunkar S. Bacillus circulans exopolysaccharide: Production, characterization and bioactivities. Int J Biol Macromol. 2016;87:405-414.

Fontaine T, Wieruszeski JM, Talmont F, Saniez MH, Duflot P, Leleu JB, Fournet B. Exopolysaccharide structure from Bacillus circulans. Eur J Biochem. 1991;196(1):107-13.

Kekez B, Gojgić-Cvijović G, Jakovljević D, Pavlović V, Beškoski V, Popović A, Vrvić MM, NikolićV.Synthesis and characterization of a new type of levan-graft-polystyrene copolymer. CarbohydrPolym. 2016;154:20-29.

Kekez BD, Gojgić-Cvijović GD, Jakovljević DM, Stefanović Kojić JR, Marković MD, 492 Beškoski VP, Vrvić MM. High Levan Production by Bacillus licheniformis NS032 Using Ammonium Chloride as the Sole Nitrogen Source. Appl BiochemBiotechnol. 2015;175(6):3068-3083.

Castillo HFD, Reyes CF, Morales GG, Herrera RR, Aguilar C. Biological Control of Root Pathogens by Plant- Growth Promoting Bacillus spp. In: Saloneski S, Larramnedy M, eds. Weed and Pest Control - Conventional and New Challenges. InTech; 2013:80-103.

Abhyankar W, Beek A Ter, Dekker H, Kort R, Brul S, de Koster CG. Gel-free proteomic identification of the Bacillus subtilis insoluble spore coat protein fraction. Proteomics. 2011;11(23):4541-4550.

Öztürk S, Çalık P, Özdamar TH. Fed-Batch Biomolecule Production by Bacillus subtilis: A State of the Art Review. Trends Biotechnol. 2016;34(4):329-345.

Galaction A-I, Oniscu C, Cascaval D. Studies on oxygen mass transfer in stirred bioreactors 2: Suspensions of bacteria, yeasts and fungis. Hem Ind. 2003;57(6):276-287.

Stamenković S, Beškoski V, Karabegović I, Lazić M, Nikolić N. Microbial fertilizers: A comprehensive review of current findings and future perspectives. Spanish J Agric Res. 2018;16(1):e09R01.

Monteiro SMS, Clemente JJ, Carrondo MJT, Cunha AE. Enhanced Spore Production of Bacillus subtilis Grown in a Chemically Defined Medium. Adv Microbiol. 2014;4(8):444-454.

Matar SM, El-Kazzaz SA, Wagih EE, El-Diwany AI, Moustafa HE, Abo Zaid GA, Hafez EE. Bioprocessing and scaling-up cultivation of Bacillus subtilis as a potential antagonist to certain plant pathogenic fungi, III. Biotechnology. 2009;8(1):138-143.

Reis A, Da Silva TL, Kent CA, Kosseva M, Roseiro JC, Hewitt CJ. Monitoring population dynamics of the thermophilic Bacillus licheniformis CCMI 1034 in batch and continuous cultures using multi-parameter flow cytometry. J Biotechnol. 2005;115(2):199-210.

Glick BR. Beneficial Plant-Bacterial Interactions. Springer International Publishing Switzerland; 2015.

Shaikh SS, Sayyed RZ. Role of Plant Growth-Promoting Rhizobacteria and Their Formulation in Biocontrol of Plant Diseases. In: Arora NK, ed. Plant Microbes Symbiosis: Applied Facets. New Delhi: Springer India; 2015:337-351.

Elsayed AE, Othman NZ, Malek RA, Awad HM, Wu K, Azizi R, Wadaan HM, Enshasy H. Bioprocess Development for High Cell Mass and Endospore Production by Bacillus thuringiensis var israelensis in Semi-Industrial Scale. J Pure Appl Microbiol. 2014;8(4):2773-2783.

Khardziani T, Kachlishvili E, Sokhadze K, Elisashvili V, ChikindasML, Chistyakov V. Elucidation of Bacillus subtilis KATMIRA 1933 Potential for Spore Production in Submerged Fermentation of Plant Raw Materials. Probiotics Antimicrob Proteins. 2017; 9 (4): 435-443.

Piggot PJ, Coote JG. Genetic aspects of bacterial endospore formation. Bacteriol Rev. 1976;40(4):908-962.

Leo Daniel A, Venkateswarlu B, Suseelendra D, et al. Effect of Polymeric Additives, Adjuvants, Surfactants on Survival, Stability and Plant Growth Promoting Ability of Liquid Bioinoculants. J Plant PhysiolPathol. 2013;1(2):1-5.

Monteiro SM, Clemente JJ, Henriques AO, Gomes RJ, Carrondo MJ, Cunha AE. A procedure for high-yield spore production by Bacillus subtilis. Biotechnol Prog. 2005;21(4):1026-1031.

Brul S, van Beilen J, Caspers M, O'Brien A, de Coster C, Oomes S, Smelt J, Kort R, Ter Beek A. Challenges and advances in systems biology analysis of Bacillus spore physiology; molecular differences between an extreme heat resistant spore forming Bacillus subtilis food isolate and a laboratory strain. Food Microbiol. 2011;28(2):221-227.

Vassilev N, Vassileva M, Lopez A, Martos V, Reyes A, Maksimovic I, Elcher-Lobermann B, Malusa E. Unexploited potential of some biotechnological techniques for biofertilizer production and formulation. Appl Microbiol Biotechnol. 2015;99(12):4983-4996.

Singhania RR, Patel AK, Soccol CR, Pandey A. Recent advances in solid-state fermentation. BiochemEng J. 2009;44(1):13-18.

Morris ON, Kanagaratnam P, Converse V. Suitability of 30 Agricultural Products and By-Products as Nutrient Sources for Laboratory Production of Bacillus thuringiensis subsp. aizawai (HD133). J InvertebrPathol. 1997;70(2):113-20.

Sánchez Blanco A, Palacios Durive O, Batista Pérez S, Díaz Montes Z, Pérez Guerra N. Simultaneous production of amylases and proteases by Bacillus subtilis in brewery wastes. Brazilian J Microbiol. 2016;47(3):665-674.

Baş D, Boyacı İH. Modeling and optimization I: Usability of response surface methodology. J Food Eng. 2007;78(3):836-845.

Montgomery DC. Design and Analysis of Experiments. John Wiley & Sons, Inc; 2001.

Rushing H, Karl A, Wisnowski J. Design and Analysis of Experiments by Douglas Montgomery: A Supplement for Using JMP(R). Cary, North Carolina, USA: SAS Institute Inc.; 2013.

Nwabueze TU. Basic steps in adapting response surface methodology as mathematical modelling for bioprocess optimisation in the food systems. Int J Food Sci Technol. 2010;45(9):1768-1776.

Karabegović IT, Stojičević SS, Veličković DT, Nikolić NČ, Lazić ML. Optimization of Microwave-Assisted Extraction of Cherry Laurel Fruit. Sep Sci Technol. 2014;49(3):416-423.

Lundstedt T, Seifert E, Abramo L, et al. Experimental design and optimization. ChemomIntell Lab Syst. 1998;42(1-2):3-40.

Ameer K, Bae S, Jo Y, Lee H, Ameer A, Kwon J. Optimization of microwave-assisted extraction of total extract, stevioside and rebaudioside-A from Stevia rebaudiana (Bertoni) leaves, using response surface methodology (RSM) and artificial neural network (ANN) modelling. Food Chem. 2017;229:198-207.

Sreekumar G, Krishnan S. Enhanced biomass production study on probiotic Bacillus subtilis SK09 by medium optimization using response surface methodology. African J Biotechnol. 2010;9(45):8078-8084.

Chen Z-M, Li Q, Liu H-M, Yu N, Xie TJ, Yang MJ, Shen P, Chen XD. Greater enhancement of Bacillus subtilis spore yields in submerged cultures by optimization of medium composition through statistical experimental designs. Appl Microbiol Biotechnol. 2010;85(5):1353-1360.

Anh NQ. Development of Bacillus Subtilis Spores and Cells for Surface Display of Proteins. Bayreuth: der FakultätfürBiologie, Chemie und Geowissenschaften der Universität Bayreuth; 2010.

Ghasemi S, Ahmadzadeh M. Optimisation of a cost-effective culture medium for the large-scale production of Bacillus subtilis UTB96. Arch Phytopathol Plant Prot. 2013;46(13):1552-1563.

Shih IL, Lin CY, Wu JY, Hsieh C. Production of antifungal lipopeptide from Bacillus subtilis in submerged fermentation using shake flask and fermentor. Korean J Chem Eng. 2009;26(6):1652-1661.

Zhao X, Han Y, Tan X qian, Wang J, Zhou Z jiang. Optimization of antifungal lipopeptide production from Bacillus sp. BH072 by response surface methodology. J Microbiol. 2014;52(4):324-332.

Mizumoto S, Shoda M. Medium optimization of antifungal lipopeptide, iturin A, production by Bacillus subtilis in solid-state fermentation by response surface methodology. Appl Microbiol Biotechnol. 2007;76(1):101-108.

Cheng S., Y.F. W, F.F. L. Optimization of Medium Compositions Using Statistical Experimental Design to Produce Lipase by Bacillus subtilis. Chem BiochemEng Q. 2011;25(3):377-383.

Tavares MB, Souza RD, Luiz WB, Cavalcante RCM, Casaroli C, Martins EG, Ferreira RCC, 584 Ferreira LCS.Bacillus subtilis endospores at high purity and recovery yields: Optimization of growth conditions and purification method. Curr Microbiol. 2013;66(3):279-285.

Bashan Y, Trejo A, de-Bashan LE. Development of two culture media for mass cultivation of Azospirillumspp. and for production of inoculants to enhance plant growth. Biol Fertil Soils. 2011;47(8):963-969.

Pryor SW, Gibson DM, Hay AG, Gossett JM, Walker LP. Optimization of spore and antifungal lipopeptide production during the solid-state fermentation of Bacillus subtilis. Appl BiochemBiotechnol. 2007;143(1):63-79.

Movahedi S, Waites W. Cold shock response in sporulating Bacillus subtilis and its effect on spore heat resistance. J Bacteriol. 2002;184(19):5275-81.

Pandey R, Pieper GH, Beek A Ter, Vischer NOE, Smelt JPPM, Manders EMM, Brul S. Quantifying the effect of sorbic acid, heat and combination of both on germination and outgrowth of Bacillus subtilis spores at single cell resolution. Food Microbiol. 2015;52:88-96.

Tzeng Y-M, Rao YK, Tsay K-J, Wu W-S. Effect of cultivation conditions on spore production from Bacillus amyloliquefaciens B128 and its antagonism to Botrytis elliptica. J Appl Microbiol. 2008;104(5):1275-1282.

Naseva O, Stamenković I, Banković-Ilić I, Lazić M, Veljković V, Skala D. Sadržaj gasa u bioreaktoru sa vibracionom mešalicom - tečnafaza je nenjutnovski fluid. HemInd. 2002;56(5):198-203. (in Serbian).

Suresh S, Srivastava VC, Mishra IM. Techniques for oxygen transfer measurement in bioreactors: A review. J Chem Technol Biotechnol. 2009;84(8):1091-1103.

Wu Z, Du G, Chen J. Effects of dissolved oxygen concentration and DO-stat feeding strategy on CoQ 10 production with Rhizobium radiobacter. World J Microbiol Biotechnol. 2003;19:925-928.

Sarrafzadeh MH, Schorr-Galindo S, La H-J, Oh H-M. Aeration effects on metabolic events during sporulation of Bacillus thuringiensis. J Microbiol. 2014;52(7):597-603.

Suresh S, Srivastava VC, Mishra IM. Critical analysis of engineering aspects of shaken flask bioreactors. Crit Rev Biotechnol. 2009;29(4):255-278.

Cascaval D, Galaction A-I, Oniscu C, Ungureanu F. Modeling of mixing in stirred bioreactors 4. Mixing time for aerated bacteria, yeasts and fungus broths. Hem Ind. 2004;56(3):128-137.

Richard A, Margaritis A. Rheology, oxygen transfer, and molecular weight characteristics of poly(glutamic acid) fermentation by Bacillus subtilis. BiotechnolBioeng. 2003;82(3):299-305.

Garcia-Ochoa F, Gomez E. Bioreactor scale-up and oxygen transfer rate in microbial processes: An overview. Biotechnol Adv. 2009;27(2):153-176.

Venkatachalam S, Palaniappan A, Kandasamy S, Kandasamy K. Prediction of gas holdup in a combined loop air lift fluidized bed reactor using Newtonian and non-Newtonian liquids. Chem Ind Chem Eng Q. 2011;17(3):375-383.

Veljković VB, Nikolić S, Lazić ML, Engler CR. Oxygen transfer in flasks shaken on orbital shakers. Hem Ind. 1995;49:265-272.

Hbid C, Jacques P, Razafindralambo H, Mpoyo MK, Meurice E, Paquot M, Thonart P. Influence of the production of two lipopeptides, Iturin a and Surfactin S1, on oxygen transfer during Bacillus subtilis fermentation. Appl BiochemBiotechnol. 1996;57-58(1):571-579.

Shih I-L, Lin C-Y, Wu J-Y, Hsieh C. Production of antifungal lipopeptide from Bacillus subtilis in submerged fermentation using shake flask and fermentor. Korean J Chem Eng. 2009;26(6):1652-1661.

Sen R, Babu KS. Modeling and optimization of the process conditions for biomass production and sporulation of a probiotic culture. Process Biochem. 2005;40(7):2531-2538.

Man Z-W, Rao Z-M, Cheng Y-P, Yang TW, Zhang X, Xu MJ, Xu ZH. Enhanced riboflavin production by recombinant Bacillus subtilis RF1 through the optimization of agitation speed. World J Microbiol Biotechnol. 2014; 30(2): 661-667.

Wang DIC, Cooney CL, Demain AL, Dunnill P, Humphrey AE, Lilly MD. Translation of laboratory, pilot, and plant scale data. Ferment Enzym Technol Wiley, New York. 1997:194-211.

Seletzky JM, Noak U, Fricke J, Welk E, Eberhard W, Knocke C, Buchs J. Scale-up from shake flasks to fermenters in batch and continuous mode with Corynebacterium glutamicum on lactic acid based on oxygen transfer and pH. Biotechnol Bioeng. 2007;98(4):800-811.

Trujillo-Roldán MA, Valdez-Cruz NA, Gonzalez-Monterrubio CF, Acevedo-Sanchez EV, Martínez-Salinas C, García-Cabrera RI, Gamboa-Suasnavart RA, Marín-Palacio LD, Villegas J, Blancas-Cabrera A. Scale-up from shake flasks to pilot-scale production of the plant growth-promoting bacterium Azospirillum brasilense for preparing a liquid inoculant formulation. Appl Microbiol Biotechnol. 2013;97(22):9665-9674.

Maier U, Losen M, Büchs J. Advances in understanding and modeling the gas-liquid mass transfer in shake flasks. BiochemEng J. 2004;17:155-167.

Meier K, Klöckner W, Bonhage B, Antonov E, Regestein L, Büchs J. Correlation for the maximum oxygen transfer capacity in shake flasks for a wide range of operating conditions and for different culture media. BiochemEng J. 2016;109:228-235.

Malusá E, Sas-Paszt L, Ciesielska J. Technologies for Beneficial Microorganisms Inocula Used as Biofertilizers. Sci World J. 2012;2012:1-12.

Chung S, Lim JH, Kim SD. Powder formulation using heat resistant endospores of two multi-functional plant growth promoting rhizobacteria Bacillus strains having phytophtora blight suppression and growth promoting functions. J Appl Biol Chem. 2010;53(4):485-492.

Gotor-Vila A, Usall J, Torres R, Abadias M, Teixidó N. Formulation of the biocontrol agent Bacillus amyloliquefaciens CPA-8 using different approaches: liquid, freeze-drying and fluid-bed spray-drying. BioControl. 2017;62(4):545-555.

Omer AM. Bioformulations of bacillus spores for using as Biofertilizer. Life Sci J. 2010;7(4):124-131.

Schoebitz M, López MD, Roldán A. Bioencapsulation of microbial inoculants for better soil-plant fertilization. A review. Agron Sustain Dev. 2013;33 (4): 1-10.

Morgan CA, Herman N, White PA, Vesey G. Preservation of micro-organisms by drying; A review. J Microbiol Methods. 2006;66(2):183-193.

Morgan C, Vesey G. Freeze-Drying of Microorganisms. Encycl Microbiol. 2009; 162-173.

Han L, Pu T, Wang X, et al. Optimization of a protective medium for enhancing the viability of freeze-dried Bacillus amyloliquefaciens B1408 based on response surface methodology. Cryobiology. 2018.

Zhan Y, Xu Q, Yang MM, et al. Screening of freeze-dried protective agents for the formulation of biocontrol strains, Bacillus cereus AR156, Burkholderiavietnamiensis B418 and Pantoeaagglomerans 2Re40. Lett Appl Microbiol. 2012;54(1):10-17.

Mahidsanan T, Gasaluck P, Eumkeb G. A novel soybean flour as a cryoprotectant in freeze-dried Bacillus subtilis SB-MYP-1. LWT - Food Sci Technol. 2017;77:152-159.

Jayasudha SM, Kirankumar KC, Mesta RK, Ippikoppa R. Liquid Formulation Using Different Oils and Shelf Life Study of Effective Bacterial Bio-Agents. IntJCurrMicrobiolAppSci. 2018;7(4):317-324.

Schisler DA, Slininger PJ, Behle RW, Jackson MA. Formulation of Bacillus spp. for Biological Control of Plant Diseases. Phytopathology. 2004;94(11):1267-1271.

Kim S-Y, Kim H-E, Kim Y-S. The potentials of Bacillus licheniformis strains for inhibition of B. cereus growth and reduction of biogenic amines in cheonggukjang (Korean fermented unsalted soybean paste). Food Control. 2017;79:87-93.

Similar Articles

You may also start an advanced similarity search for this article.