Microencapsulated biofertilizer formulation: product development and effect on growth of green pepper seedlings

Sandra Stamenković Stojanović; Ivana Karabegović; Bojana Danilović; Viktor Nedović; Ana Kalušević; Stojan Mančić; Midrag  Lazić

doi:10.5424/sjar/2022203-19062

Sandra Stamenković Stojanović University of Niš, Faculty of Technology, Bulevar Oslobodjenja 124, 16000 Leskovac, Serbia https://orcid.org/0000-0001-6706-9318
Ivana Karabegović University of Niš, Faculty of Technology, Bulevar Oslobodjenja 124, 16000 Leskovac, Serbia https://orcid.org/0000-0003-2191-4082
Bojana Danilović University of Niš, Faculty of Technology, Bulevar Oslobodjenja 124, 16000 Leskovac, Serbia https://orcid.org/0000-0002-4444-2746
Viktor Nedović University of Belgrade, Faculty of Agriculture, Nemanjina 6, 11080 Belgrade, Serbia https://orcid.org/0000-0002-8943-0087
Ana Kalušević Academy of Applied Studies Belgrade, Zoran Djindjic Bl. 152a, 11070 Belgrade, Serbia https://orcid.org/0000-0002-4343-9246
Stojan Mančić University of Niš, Faculty of Technology, Bulevar Oslobodjenja 124, 16000 Leskovac, Serbia https://orcid.org/0000-0001-9952-1575
Midrag Lazić University of Niš, Faculty of Technology, Bulevar Oslobodjenja 124, 16000 Leskovac, Serbia https://orcid.org/0000-0002-6634-7686

DOI: https://doi.org/10.5424/sjar/2022203-19062

Keywords: plant growth promotion, optimization, phytostimulation, Bacillus subtilis

Abstract

Aim of the study: This study aimed to formulate a novel, commercially applicable biofertilizer, to optimize the microencapsulation procedure of Bacillus subtilis NCIM 2063 and examine the stability and phytostimulatory effects of obtained formulation.

Area of the study: Southestern Serbia.

Material and methods: Microbial powder formulations were prepared using spray drying with maltodextrin as a carrier. The spray drying conditions were set according to Box-Benkhen experimental desing. The effect of the formulation was tested on green pepper (Capsicum annuum) seeds in controled conditions.

Main results: Response surface models were developed. All of the models were statistically significant, adequately fitted and reproducible. The maximum achieved values of viability and yield in a formulation were 1.99·10⁹ CFU/g and 96.8%, respectively, whilst the driest formulation had 1.44% moisture. The following optimum conditions were proposed for the spray drying procedure: an inlet air temperature of 133 °C, maltodextrin concentration of 50 g/L and a feed flow rate of 6.5 mL/min. The obtained microbial formulation had a high survival rate after being stored at room temperature over a 1--year period. Its application on green pepper seeds had beneficial effect on plant height, leaf dry weight and chlorophyll content of the seedlings.

Research highlights: B. subtilis was successfully microencapsulated on maltodextrin as a carrier. Interaction effects between the process variables were fully explained and statistically significant models were developed. In addition to biocontrol properties formulation had a phytostimulatory effect, excellent stability and satisfactory physical properties.

Downloads

Download data is not yet available.

References

Adhikari B, Howes T, Lecomte D, Bhandari BR, 2005. A glass transition temperature approach for the prediction of the surface stickiness of a drying droplet during spray drying. Powder Technol 149: 168-179. https://doi.org/10.1016/j.powtec.2004.11.007

Adjallé KD, Vu KD, Tyagi RD, Brar SK, Valéro JR, Surampalli RY, 2011. Optimization of spray drying process for Bacillus thuringiensis fermented wastewater and wastewater sludge. Bioprocess Biosyst Eng 34: 237-246. https://doi.org/10.1007/s00449-010-0466-y

Amiet-Charpentier C, Gadille P, Digat B, Benoit JP, 1998. Microencapsulation of rhizobacteria by spray-drying: Formulation and survival studies. J Microencapsul 15: 639-659. https://doi.org/10.3109/02652049809008247

Bakar J, Ee SC, Muhammad K, Hashim DM, Adzahan N, 2013. Spray-drying optimization for red pitaya peel (Hylocereus polyrhizus). Food Bioprocess Technol 6: 1332-1342. https://doi.org/10.1007/s11947-012-0842-5

Barcelos GS, Dias LC, Fernandes PL, Fernandes R de CR., Borges AC, Kalks KHM, Tótola MR, 2014. Spray drying as a strategy for biosurfactant recovery, concentration and storage. Springerplus 3: 1-9. https://doi.org/10.1186/2193-1801-3-49

Baş D, Boyacı İH, 2007. Modeling and optimization I: Usability of response surface methodology. J Food Eng 78: 836-845. https://doi.org/10.1016/j.jfoodeng.2005.11.024

Behboudi-Jobbehdar S, Soukoulis C, Yonekura L, Fisk I, 2013. Optimization of spray-drying process conditions for the production of maximally viable microencapsulated L. acidophilus NCIMB 701748. Dry Technol 31: 1274-1283. https://doi.org/10.1080/07373937.2013.788509

Ben Khedher S, Mejdoub-Trabelsi B, Tounsi S, 2021. Biological potential of Bacillus subtilis V26 for the control of Fusarium wilt and tuber dry rot on potato caused by Fusarium species and the promotion of plant growth. Biol Control 152: 104444. https://doi.org/10.1016/j.biocontrol.2020.104444

Bhagwat A, Bhushette P, Annapure US, 2020. Spray drying studies of probiotic Enterococcus strains encapsulated with whey protein and maltodextrin. Beni-Suef Univ. J Basic Appl Sci 9: 1-15. https://doi.org/10.1186/s43088-020-00061-z

Campos DC, Acevedo F, Morales E, Aravena J, Amiard V, Jorquera MA, Inostroza NG, Rubilar M. 2014. Microencapsulation by spray drying of nitrogen-fixing bacteria associated with lupin nodules. World J Microbiol Biotechnol 30: 2371-2378. https://doi.org/10.1007/s11274-014-1662-8

Chauhan H, Bagyaraj DJ, Selvakumar G, Sundaram SP, 2015. Novel plant growth promoting rhizobacteria-Prospects and potential. Appl Soil Ecol 95: 38-53. https://doi.org/10.1016/j.apsoil.2015.05.011

Derringer G, Suich R, 1980. Simultaneous optimization of several response variables. J Qual Technol 12: 214-219. https://doi.org/10.1080/00224065.1980.11980968

Garcia AL, Madrid R, Gimeno V, Rodriguez-Ortega WM, Nicolas N, Garcia-Sanchez F, 2011. The effects of amino acids fertilization incorporated to the nutrient solution on mineral composition and growth in tomato seedlings. Span J Agric Res 9: 852-861. https://doi.org/10.5424/sjar/20110903-399-10

Hashem A, Tabassum B, Fathi Abd E, 2019. Bacillus subtilis: A plant-growth promoting rhizobacterium that also impacts biotic stress. Saudi J Biol Sci 26: 1291-1297. https://doi.org/10.1016/j.sjbs.2019.05.004

Hiscox JD, Israelstam GF, 1979. A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57: 1332-1334. https://doi.org/10.1139/b79-163

Huang S, Vignolles ML, Chen XD, Le Loir Y, Jan G, Schuck P, Jeantet R, 2017. Spray drying of probiotics and other food-grade bacteria: A review. Trends Food Sci Technol 63: 1-17. https://doi.org/10.1016/j.tifs.2017.02.007

Hussain N, Abbasi T, Abbasi SA, 2017. Detoxification of parthenium (Parthenium hysterophorus) and its metamorphosis into an organic fertilizer and biopesticide. Bioresour Bioprocess 4: 1-9. https://doi.org/10.1186/s40643-017-0156-6

Keswani C, Bisen K, Singh V, Sarma BK, Singh HB, 2016. Formulation technology of biocontrol agents: present status and future prospects. In: Bioformulations for sustainable agriculture (Arora NK & Mehnaz S, eds). Springer, New Delhi, India, pp: 35-52. https://doi.org/10.1007/978-81-322-2779-3_2

Ma X, Wang X, Cheng J, Nie X, Yu X, Zhao Y, Wang W, 2015. Microencapsulation of Bacillus subtilis B99-2 and its biocontrol efficiency against Rhizoctonia solani in tomato. Biol Control 90: 1-10. https://doi.org/10.1016/j.biocontrol.2015.05.013

Malićanin M, Danilović B, Cvetković D, Stamenković-Stojanović S, Nikolić N, Lazić M, Karabegović I, 2020. Modulation of aroma and sensory properties of Prokupac wines by a Bacillus-based preparation applied to grapes prior to harvest. South Afr J Enol Vitic 41: 158-167. https://doi.org/10.21548/41-2-4016

Meng X, Yu J, Yu M, Yin X., Liu Y, 2015. Dry flowable formulations of antagonistic Bacillus subtilis strain T429 by spray drying to control rice blast disease. Biol Control 85: 46-51. https://doi.org/10.1016/j.biocontrol.2015.03.004

Mousivand M, Salehi Jouzani GH, Hashemi M, 2012. Biofilm formation improved the biocontrol of Bacillus subtilis against Fusarium head blight. N Biotechnol 29: S23. https://doi.org/10.1016/j.nbt.2012.08.058

Nedovic V, Kalusevic A, Manojlovic V, Levic S, Bugarski B, 2011. An overview of encapsulation technologies for food applications. Procedia Food Sci 1: 1806-1815. https://doi.org/10.1016/j.profoo.2011.09.265

Nedović V, Kalušević A, Manojlović V, Petrović T, Bugarski B, 2013. Encapsulation systems in the food industry. In: Advances in food process engineering research and applications; Yanniotis S et al. (eds.), pp: 229-253. Springer, Boston. https://doi.org/10.1007/978-1-4614-7906-2_13

Peighambardoust SH, Golshan Tafti A, Hesari J, 2011. Application of spray drying for preservation of lactic acid starter cultures: A review. Trends Food Sci Technol 22: 215-224. https://doi.org/10.1016/j.tifs.2011.01.009

Rodrigues AC, Fontão AI, Coelho A, Leal M, Soares da Silva FAG, Wan Y et al., 2019. Response surface statistical optimization of bacterial nanocellulose fermentation in static culture using a low-cost medium. N Biotechnol 49: 19-27. https://doi.org/10.1016/j.nbt.2018.12.002

Samaniego-Gámez BY, Garruña R, Tun-Suárez JM, Kantun-Can J, Reyes-Ramírez A, Cervantes-Díaz L, 2016. Bacillus spp. inoculation improves photosystem II efficiency and enhances photosynthesis in pepper plants. Chil J Agr Res 76: 409-416. https://doi.org/10.4067/S0718-58392016000400003

Schuck P, 2009. Understanding the factors affecting spray-dried dairy powder properties and behavior. In: Dairy-derived ingredients: food and nutraceutical uses. pp: 24-50. Elsevier Ltd. https://doi.org/10.1533/9781845697198.1.24

Seth D, Mishra HN, Deka SC, 2017. Effect of spray drying process conditions on bacteria survival and acetaldehyde retention in sweetened yoghurt powder: An optimization study. J Food Process Eng 40: 1-10. https://doi.org/10.1111/jfpe.12487

Sonbarse PP, Kiran K, Sharma P, Parvatam G, 2020. Biochemical and molecular insights of PGPR application for the augmentation of carotenoids, tocopherols, and folate in the foliage of Moringa oleifera. Phytochemistry 179: 112506. https://doi.org/10.1016/j.phytochem.2020.112506

Stamenković S, Beškoski V, Karabegović I, Lazić M, Nikolić N, 2018. Microbial fertilizers: A comprehensive review of current findings and future perspectives. Span J Agric Res 16: e09R01. https://doi.org/10.5424/sjar/2018161-12117

Stamenkovic-Stojanovic S, Karabegovic I, Beskoski V, Nikolic N, Lazic M, 2019. Bacillus based microbial formulations: Optimization of the production process. Hem Ind 73: 169-182. https://doi.org/10.2298/HEMIND190214014S

Swain MR, Naskar SK, Ray RC, 2007. Indole-3-acetic acid production and effect on sprouting of yam [Dioscorea rotundata L.] minisetts by Bacillus subtilis isolated from culturable cowdung microflora. Polish J Microbiol 56: 5-15.

Tao S, Wu Z, Wei M, Liu X, He Y, Ye BC, 2019. Bacillus subtilis SL-13 biochar formulation promotes pepper plant growth and soil improvement. Can J Microbiol 65: 333-342. https://doi.org/10.1139/cjm-2018-0333

Vassilev N, Vassileva M, Lopez A, Martos V, Reyes A, Maksimovic I et al., 2015. Unexploited potential of some biotechnological techniques for biofertilizer production and formulation. Appl Microbiol Biotechnol 99: 4983-4996. https://doi.org/10.1007/s00253-015-6656-4

Wang H, Jiang K, Zhu Z, Jiang W, Yang Z, Zhu S et al., 2018. Optimization of fed-batch fermentation and direct spray drying in the preparation of microbial inoculant of acetochlor-degrading strain Sphingomonas sp. DC-6. 3 Biotech 8: 1-9. https://doi.org/10.1007/s13205-018-1324-x

Yánez-Mendizábal V, Viñas I, Usall J, Torres R, Solsona C, Abadias M, Teixidó N, 2012. Formulation development of the biocontrol agent Bacillus subtilis strain CPA-8 by spray-drying. J Appl Microbiol 112: 954-965. https://doi.org/10.1111/j.1365-2672.2012.05258.x

Yu X, Ai C, Xin L, Zhou G, 2011. The siderophore-producing bacterium, Bacillus subtilis CAS15, has a biocontrol effect on Fusarium wilt and promotes the growth of pepper. Eur J Soil Biol 47: 138-145. https://doi.org/10.1016/j.ejsobi.2010.11.001

Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW, 2008. Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56: 264-273. https://doi.org/10.1111/j.1365-313X.2008.03593.x