Abstract
Currently, the growing demand for non-dairy functional foods leads to the constant development of new products. The objective of the present work was to obtain a soy-based fermented beverage employing the strains Lactiplantibacillus plantarum CIDCA 8327 or Lacticaseibacillus paracasei BGP1 and to analyze the effect of post-fermentation addition of inulin of low or high average polymerization degree on the bacterial resistance. Also, the antimicrobial and antioxidant activity of the fermented soy-based beverages were analyzed. The soy-based matrix was shown to be a suitable substrate for the growth of both lactic acid bacteria, and the fermented beverages obtained presented bioactive properties such us antioxidant activity and bactericidal effect against pathogen microorganisms. The addition of inulin after the fermentation process avoid the hydrolysis and so, preserve its polymerization degree and thus the potential prebiotic effect. The incorporation of inulin to the soy-based fermented beverages increased the bacterial count after 30 days of refrigerated storage up to 8.71 ± 0.15 and 8.41 ± 0.10 log CFU/mL for L. paracasei and L. planatrum respectively. The resistance to the gastrointestinal conditions of the strain L. paracasei BGP1 in the fermented beverage was improved up to 70% when inulin of high polymerization degree was added. Meanwhile the strain L. plantarum CIDCA 8327 showed a survival of 97 and 94% in the fermented beverage added with inulin of low or high polymerization degree, respectively. These results contribute to the development of non-dairy products containing inulin and probiotics and the diversification agri-based functional foods.
Graphical abstract
Similar content being viewed by others
References
Aguirre L, Hebert EM, Garro MS, de Giori GS (2014) Proteolytic activity of Lactobacillus strains on soybean proteins. LWT-Food Sci Technol 59(2):780–785. https://doi.org/10.1016/j.lwt.2014.06.061
Bao Y, Zhang Y, Li H, Liu Y, Wang S, Dong X, Su F, Yao G, Sun T, Zhang H (2012) In vitro screen of Lactobacillus plantarum as probiotic bacteria and their fermented characteristics in soymilk. Ann Microbiol 62(3):1311–1320. https://doi.org/10.1007/s13213-011-0377-4
Battistini C, Gullón B, Ichimura ES, Gomes AMP, Ribeiro EP, Kunigk L et al (2018) Development and characterization of an innovative synbiotic fermented beverage based on vegetable soybean. Braz J Microbiol 49(2):303–309. https://doi.org/10.1016/j.bjm.2017.08.006
Bedani R, Rossi EA, Isay Saad SM (2013) Impact of inulin and okara on Lactobacillus acidophilus La-5 and Bifidobacterium animalis bb-12 viability in a fermented soy product and probiotic survival under in vitro simulated gastrointestinal conditions. Food Microbiol 34(2):382–389. https://doi.org/10.1016/j.fm.2013.01.012
Bergsveinson J, Kajala I, Ziola B (2017) Next-generation sequencing approaches for improvement of lactic acid bacteria-fermented plant-based beverages. AIMS Microbiol 3(1):8. https://doi.org/10.3934/microbiol.2017.1.8
Bernat N, Cháfer M, Chiralt A, González-Martínez C (2014) Hazelnut milk fermentation using probiotic Lactobacillus rhamnosus GG and inulin. Int J Food Sci Technol 49(12):2553–2562. https://doi.org/10.1111/ijfs.12585
Bian L, Molan AL, Maddox I, Shu Q (2011) Antimicrobial activity of Lactobacillus reuteri DPC16 supernatants against selected food borne pathogens. World J Microbiol Biotechnol 27(4):991–998. https://doi.org/10.1007/s11274-010-0543-z
Brand-Williams W, Cuvelier ME, Berset CLWT (1995) Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci Technol 28(1):25–30. https://doi.org/10.1016/S0023-6438(95)80008-5
Buriti FC, Castro IA, Saad SM (2010) Effects of refrigeration, freezing and replacement of milk fat by inulin and whey protein concentrate on texture profile and sensory acceptance of symbiotic guava mousses. Food Chem 123(4):1190–1197. https://doi.org/10.1016/j.foodchem.2010.05.085
Capriotti AL, Caruso G, Cavaliere C, Samperi R, Ventura S, Chiozzi RZ, Laganà A (2015) Identification of potential bioactive peptides generated by simulated gastrointestinal digestion of soybean seeds and soy milk proteins. J Food Comp Anal Aci 44:205–213. https://doi.org/10.1016/j.jfca.2015.08.007
Céspedes M, Cárdenas P, Staffolani M, Ciappini M, Vinderola G (2013) Performance in nondairy drinks of probiotic L. casei strains usually employed in dairy products. J Food Sci 78(5):756–762
de Souza Oliveira RP, Perego P, Converti A, De Oliveira MN (2009) The effect of inulin as a prebiotic on the production of probiotic fibre-enriched fermented milk. Int J Dairy Tech 62(2):195–203. https://doi.org/10.1111/j.1471-0307.2009.00471.x
Donkor ON, Henriksson A, Vasiljevic T, Shah NP (2007a) Rheological properties and sensory characteristics of set-type soy yogurt. J Agric Food Chem 55(24):9868–9876. https://doi.org/10.1021/jf071050r
Donkor ON, Henriksson A, Vasiljevic T, Shah NP (2007b) α-Galactosidase and proteolytic activities of selected probiotic and dairy cultures in fermented soymilk. Food Chem 104(1):10–20. https://doi.org/10.1016/j.foodchem.2006.10.065
dos Santos DC, de Oliveira Filho JG, Santana ACA, de Freitas BSM, Silva FG, Takeuchi KP, Egea MB (2019) Optimization of soymilk fermentation with kefir and the addition of inulin: physicochemical, sensory and technological characteristics. LWT-Food Sci Technol 104:30–37. https://doi.org/10.1016/j.lwt.2019.01.030
Ebhodaghe SO, Abiose SH, Adeniran HA (2012) Assessment of physico–chemical characteristics, viability and inhibitory effect of Bifidobacteria in soymilk. J Food Res 1(2):159. https://doi.org/10.5539/jfr.v1n2p159
Farnworth ER, Mainville I, Desjardins MP, Gardner N, Fliss I, Champagne C (2007) Growth of probiotic bacteria and bifidobacteria in a soy yogurt formulation. Int J Food Microbiol 116(1):174–181. https://doi.org/10.1016/j.ijfoodmicro.2006.12.015
Fukuda M, Kobayashi M, Honda Y (2017) Functional components and health benefits of fermented soymilk in soft chem. Food Ferm. https://doi.org/10.1016/B978-0-12-811412-4.00006-0
Gangoiti MV, Puertas AI, Hamet MF, Peruzzo PJ, Llamas MG, Medrano M, Abraham AG (2017) Lactobacillus plantarum CIDCA 8327: An α-glucan producing-strain isolated from kefir grains. Carbohyd Polym 170:52–59
Garrote GL, Abraham AG, De Antoni GL (2001) Chemical and microbiological characterisation of kefir grains. J Dairy Res 68(4):639–652. https://doi.org/10.1017/S0022029901005210
Golowczyc MA, Gugliada MJ, Hollmann A, Delfederico L, Garrote GL, Abraham AG, Semorile L, De Antoni G (2008) Characterization of homofermentative lactobacilli isolated from kefir grains: potential use as probiotic. J Dairy Res 75(2):211–217. https://doi.org/10.1017/S0022029908003117
Granato D, Branco GF, Nazzaro F, Cruz AG, Faria JA (2010) Functional foods and non-dairy probiotic food development: trends, concepts, and products. Compr Rev Food Sci F 9(3):292–302. https://doi.org/10.1111/j.1541-4337.2010.00110.x
Granato D, Masson ML, Ribeiro JCB (2012) Sensory acceptability and physical stability evaluation of a prebiotic soy-based dessert developed with passion fruit juice. Food Sci Technol 32(1):119–126. https://doi.org/10.1590/S0101-20612012005000004
Grimoud J, Durand H, Courtin C, Monsan P, Ouarné F, Theodorou V, Roques C (2010) In vitro screening of probiotic lactic acid bacteria and prebiotic glucooligosaccharides to select effective synbiotics. Anaerobe 6(5):493–500. https://doi.org/10.1016/j.anaerobe.2010.07.005
Guo Z, Wang J, Yan L, Chen W, Liu XM, Zhang HP (2009) In vitro comparison of probiotic properties of Lactobacillus casei Zhang, a potential new probiotic, with selected probiotic strains. LWT-Food Sci Technol 42(10):1640–1646. https://doi.org/10.1016/j.lwt.2009.05.025
Hati S, Patel N, Mandal S (2018) Comparative growth behaviour and biofunctionality of lactic acid bacteria during fermentation of soy milk and bovine milk. Prob Antimicrob 10(2):277–283. https://doi.org/10.1007/s12602-017-9279-5
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Berni Canani R, Flint HJ, Salminen S, Calder PC, Sanders ME (2014) The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 11(8):506–514. https://doi.org/10.1038/nrgastro.2014.66
Iraporda C, Rubel IA, Manrique GD, Abraham AG (2019) Influence of inulin rich carbohydrates from Jerusalem artichoke (Helianthus tuberosus L.) tubers on probiotic properties of Lactobacillus strains. LWT-Food Sci Technol 101:738–746. https://doi.org/10.1016/j.lwt.2018.11.074
Khorasany S, Shahdadi F (2021) Improvements in survival of probiotic bacteria, rheology and sensory characteristics of yogurts during storage. Nutr Food Sci Res 8(1):35–43
Kolida S, Tuohy K, Gibson GR (2002) Prebiotic effects of inulin and oligofructose. Br J Nutr 87(2):193–197. https://doi.org/10.1079/BJN/2002537
Kumari P, Vij S (2015) Growth and antimicrobial activity of proteolytic probiotic Lactobacillus rhamnosus C6 in soymilk and whey. Indian J Dairy Sci 68(3):229–238
Londero A, Iraporda C, Garrote GL, Abraham AG (2015) Cheese whey fermented with kefir micro-organisms: antagonism against Salmonella and immunomodulatory capacity. Int J Dairy Technol 68(1):118–126
Marazza JA, Nazareno MA, de Giori GS, Garro MS (2012) Enhancement of the antioxidant capacity of soymilk by fermentation with Lactobacillus rhamnosus. J Funct Foods 4(3):594–601. https://doi.org/10.1016/j.jff.2012.03.005
Min M, Bunt CR, Mason SL, Hussain MA (2018) Non-dairy probiotic food products: an emerging group of functional foods. Crit Rev Food Sci Nutr 59(16):2626–2641
Mishra S, Mishra HN (2013) Effect of synbiotic interaction of fructooligosaccharide and probiotics on the acidification profile, textural and rheological characteristics of fermented soy milk. Food Bioproc Tech 6(11):3166–3176. https://doi.org/10.1007/s11947-012-1021-4
Mishra S, Mishra HN (2018) Comparative study of the synbiotic effect of inulin and fructooligosaccharide with probiotics with regard to the various properties of fermented soy milk. Food Sci Technol Int 24(7):564–575. https://doi.org/10.1177/1082013218776529
Monajjemi M, Aminin AN, Ilkhani AR, Mollaamin F (2012) Nano study of antioxidant activities of fermented soy whey prepared with lactic acid bacteria and kefir. Afr J Microbiol Res 6(2):426–430. https://doi.org/10.5897/AJMR11.1249
Oliveira RPDS, Perego P, De Oliveira MN, Converti A (2011) Effect of inulin as a prebiotic to improve growth and counts of a probiotic cocktail in fermented skim milk. LWT-Food Sci Technol 44(2):520–523. https://doi.org/10.1016/j.lwt.2010.08.024
Papadimitriou K, Alegría Á, Bron PA, De Angelis M, Gobbetti M, Kleerebezem M, Kok J (2016) Stress physiology of lactic acid bacteria. Microbiol Mol Biol Rev 80(3):837–890. https://doi.org/10.1128/MMBR.00076-15
Raja A, Gajalaksshmi P, Raja MMM, Imran MM (2009) Effect of Lactobacillus lactis cremoris isolated from kefir against food spoilage bacteria. Am J Food Technol 4(5):201–209. https://doi.org/10.3923/ajft.2009.201.209
Rani VU, Pradeep BV (2015) Antioxidant properties of soy milk fermented with Lactobacillus paracasei KUMB B005. Int J Pharm Sci Rev Res 30(1):39–42
Rekha CR, Vijayalakshmi G (2011) Isoflavone phytoestrogens in soymilk fermented with β-glucosidase producing probiotic lactic acid bacteria. Int J Food Sci Nutr 62(2):111–120. https://doi.org/10.3109/09637486.2010.513680
Saarela M, Virkajarvi I, Nohynek L, Vaari A, Matto J (2006) Fibres as carriers for Lactobacillus rhamnosus during freeze-drying and storage in apple juice and chocolate-coated breakfast cereals. Int J Food Microbiol 112(2):171–178. https://doi.org/10.1016/j.ijfoodmicro.2006.05.019
Saito VST, Dos Santos TF, Vinderola CG, Romano C, Nicoli JR, Araújo LS et al (2014) Viability and resistance of lactobacilli isolated from cocoa fermentation to simulated gastrointestinal digestive steps in soy yogurt. J Food Sci 79(2):M208–M213. https://doi.org/10.1111/1750-3841.12326
Schwab C, Vogel R, Gänzle MG (2007) Influence of oligosaccharides on the viability and membrane properties of Lactobacillus reuteri TMW1.106 during freeze-drying. Cryobiology 55(2):108–114
Shimakama Y, Matsubara S, Yuki N, Ikeda M, Ishikawa F (2003) Evaluation of Bifidobacterium breves strain Yakult fermented soymilk as a probiotic food. Int J Food Microbiol 81(2):131–136. https://doi.org/10.1016/S0168-1605(02)00224-6
Shokryazdan P, Sieo CC, Kalavathy R, Liang JB, Alitheen NB, Faseleh Jahromi M, Ho YW (2014) Probiotic potential of Lactobacillus strains with antimicrobial activity against some human pathogenic strains. BioMed Res Int. https://doi.org/10.1155/2014/927268
Silvestroni A, Connes C, Sesma F, De Giori GS, Piard JC (2002) Characterization of the melA locus for α-galactosidase in Lactobacillus plantarum. Appl Environ Microbiol 68(11):5464–5471. https://doi.org/10.1128/AEM.68.11.5464-5471.2002
Simova E, Beshkova D, Angelov A, Hristozova T, Frengova G, Spasov Z (2002) Lactic acid bacteria and yeasts in kefir grains and kefir made from them. J Ind Microbiol Biotechnol 28(1):1–6. https://doi.org/10.1038/sj/jim/7000186
Singh BP, Vij S, Hati S, Singh D, Kumari P, Minj J (2015) Antimicrobial activity of bioactive peptides derived from fermentation of soy milk by Lactobacillus plantarum C2 against common foodborne pathogens. Int J Ferm Foods 4(1):91–99
Souza G, De OL, Vetra AJ (1991) Acceptability of the flavour of soy bean milk yoghurt with added cow milk. Dairy Sci Abst 13(9):729
Valero-Cases E, Frutos MJ (2017) Effect of inulin on the viability of L. plantarum during storage and in vitro digestion and on composition parameters of vegetable fermented juices. Plant Foods Hum Nutr 72(2):161–167. https://doi.org/10.1007/s11130-017-0601-x
Wang YC, Yu RC, Chou CC (2002) Growth and survival of bifidobacteria and lactic acid bacteria during the fermentation and storage of cultured soymilk drinks. Food Microbiol 19(5):501–508. https://doi.org/10.1006/fmic.2002.0506
Wang YC, Yu RC, Chou CC (2006) Antioxidative activities of soymilk fermented with lactic acid bacteria and bifidobacteria. Food Microbiol 23(2):128–135. https://doi.org/10.1016/j.fm.2005.01.020
Zhao D, Shah NP (2014) Changes in antioxidant capacity, isoflavone profile, phenolic and vitamin contents in soymilk during extended fermentation. LWT-Food Sci Technol 58(2):454–462. https://doi.org/10.1016/j.lwt.2014.03.029
Acknowledgements
CI, IAR, GGL and AGA are researchers of the National Council for Scientific and Technical Research (CONICET, Argentina), GDM is member of the research career from the Scientific Research Commission (CIC, Argentina), and NM is graduated of the National University of the Center of Buenos Aires Province (UNCPBA, Argentina). Authors are grateful to Laboratorio 9 de Julio (Argentina) for pathogen microbial cultures supply.
Funding
Financial support was provided by the National Council for Scientific and Technical Research (CONICET, Argentina) and National Agency fos Scientific and Technological Promotion (ANPCyT, Argentina) PICT-2019-1220 and PICT-2019–0211.
Author information
Authors and Affiliations
Contributions
CI and IAR have made substantial contributions to conception and design, acquisition, analysis and interpretation of data, and manuscript writing. NM performed the experimental assays. GDM, GLG and AGA have been involved in drafting the manuscript and revising it critically for important intellectual content and final approval of the version to be published.
Corresponding author
Ethics declarations
Conflict of interest
The authors declared no potential conflict of interest with respect to the research, authorship, and/or publication of this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Iraporda, C., Rubel, I.A., Managó, N. et al. Inulin addition improved probiotic survival in soy-based fermented beverage. World J Microbiol Biotechnol 38, 133 (2022). https://doi.org/10.1007/s11274-022-03322-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-022-03322-4