Abstract
The waste and by-products of the soybean industry could be an economic source of nutrients to satisfy the high nutritional demands for the cultivation of lactic acid bacteria. The aims of this work were to maximize the biomass production of Lacticaseibacillus paracasei 90 (L90) in three culture media formulated from an effluent derived from soy protein concentrate production and to assess the effects these media have on the enzymatic activity of L90, together with their influence on its fermentation profile in milk. The presence of essential minerals and fermentable carbohydrates (sucrose, raffinose, and stachyose) in the effluent was verified. L90 reached high levels of microbiological counts (∼ 9 log cfu mL−1) and dry weight (> 1 g L−1) on the three optimized media. Enzymatic activities (lactate dehydrogenase and β-galactosidase) of L90, and its metabolism of lactose and citric acid, as well as lactic acid and pyruvic acid production in milk, were modified depending on the growth media. The ability of the L90 to produce the key flavour compounds (diacetyl and acetoin) was maintained or improved by growing in the optimized media in comparison with MRS.
Similar content being viewed by others
Data availability
All data generated or analysed during this study are included in this article and its supplementary information files.
References
Ahmad T, Aadil RM, Ahmed H, Rahman U, Soares BCV, Souza SLQ, Pimentel TC, Scudino H, Guimarães JT, Esmerino EA, Freitas MQ, Almada RB, Vendramel SMR, Silva MC, Cruz AG (2019) Treatment and utilization of dairy industrial waste: a review. Trends Food Sci Technol 88:361–372. https://doi.org/10.1016/j.tifs.2019.04.003
Al Loman A, Ju LK (2016) Soybean carbohydrate as fermentation feedstock for production of biofuels and value-added chemicals. Process Biochem 51:1046–1057. https://doi.org/10.1016/j.procbio.2016.04.011
Andreevskaya M, Johansson P, Jääskeläinen E, Rämö T, Ritari J, Paulin L, Björkroth J, Auvinen P (2016) Lactobacillus oligofermentans glucose, ribose and xylose transcriptomes show higher similarity between glucose and xylose catabolism-induced responses in the early exponential growth phase. BMC Genomics 17:1–18. https://doi.org/10.1186/s12864-016-2840-x
Böhmer N, König S, Fischer L (2013) A novel manganese starvation-inducible expression system for Lactobacillus plantarum. FEMS Microbiol Lett 342:37–44. https://doi.org/10.1111/1574-6968.12105
Chua J-Y, Liu S-Q (2019) Soy whey: more than just wastewater from tofu and soy protein isolate industry. Trends Food Sci Technol 91:24–32. https://doi.org/10.1016/j.tifs.2019.06.016
Cocaign-Bousquet M, Garrigues C, Loubiere P, Lindley ND (1996) Physiology of pyruvate metabolism in Lactococcus lactis. Antonie Leeuwenhoek 70:253–267. https://doi.org/10.1007/BF00395936
Coghetto CC, Vasconcelos CB, Brinques GB, Ayub MA (2016) Lactobacillus plantarum BL011 cultivation in industrial isolated soybean protein acid residue. Braz J Microbiol 47:941–948. https://doi.org/10.1016/j.bjm.2016.06.003
Crow V, Curry B, Hayes M (2001) The ecology of non-starter lactic acid bacteria (NSLAB) and their use as adjuncts in New Zealand Cheddar. Int Dairy J 11:275–283. https://doi.org/10.1016/S0958-6946(01)00057-7
Daryaei H, Coventry J, Versteeg C, Sherkat F (2010) Effects of high pressure treatment on glycolytic enzymes of Lactococcus lactis subsp. lactis, Streptococcus thermophilus and Lactobacillus acidophilus. Innov Food Sci Emerg Technol 11:245–249. https://doi.org/10.1016/j.ifset.2009.11.004
De Angelis M, Corsetti A, Tosti N, Rossi J, Corbo MR, Gobbetti M (2001) Characterization of non-starter lactic acid bacteria from Italian Ewe cheeses based on phenotypic, genotypic, and cell wall protein analyses. Appl Environ Microbiol 67:2011–2020. https://doi.org/10.1128/AEM.67.5.2011-2020.2001
Desai A, Small D, Mcgill A, Shah N (2002) Metabolism milk and of raffinose of n-hexanal stachyose in reconstituted skim and pentanal in soymilk. Biosci Microflora 21:245–250. https://doi.org/10.12938/bifidus1996.21.245
Ewe JA, Wan-Abdullah WN, Liong MT (2010) Viability and growth characteristics of Lactobacillus in soymilk supplemented with B-vitamins. Int J Food Sci Nutr 61:87–107. https://doi.org/10.3109/09637480903334163
Fei Y, Li L, Chen L, Zheng Y, Yu B (2018) High-throughput sequencing and culture-based approaches to analyze microbial diversity associated with chemical changes in naturally fermented tofu whey, a traditional Chinese tofu-coagulant. Food Microbiol 76:69–77. https://doi.org/10.1016/j.fm.2018.04.004
Fitzpatrick JJ, Ahrens M, Smith S (2001) Effect of manganese on Lactobacillus casei fermentation to produce lactic acid from whey permeate. Process Biochem 36:671–675. https://doi.org/10.1016/S0032-9592(00)00265-X
Frankowski KM, Miracle RE, Drake MA (2014) The role of sodium in the salty taste of permeate. J Dairy Sci 97:5356–5370. https://doi.org/10.3168/jds.2014-8057
Gänzle MG, Follador R (2012) Metabolism of oligosaccharides and starch in lactobacilli: a review. Front Microbiol 3(340):1–15. https://doi.org/10.3389/fmicb.2012.00340
Gao X, Qiao SY, Lu WQ (2009) Determination of an economical medium for growth of Lactobacillus fermentum using response surface methodology. Lett Appl Microbiol 49:556–561. https://doi.org/10.1111/j.1472-765X.2009.02705.x
García-Quintáns N, Blancato V, Repizo G, Magni C, López P (2008) Citrate metabolism and aroma compound production in lactic acid bacteria. In: Mayo B, López P, Pérez-Martín G (eds) Molecular aspects of lactic acid bacteria for traditional and new applications. Research Signpost, Kerala, pp 64–88
Goh YJ, Lee JH, Hutkins RW (2007) Functional analysis of the fructooligosaccharide utilization operon in Lactobacillus paracasei 1195. Appl Environ Microbiol 73:5716–5724. https://doi.org/10.1128/AEM.00805-07
González de Llano D, Rodriguez A, Cuesta P (1996) Effect of lactic starter cultures on the organic acid composition of milk and cheese during ripening-analysis by HPLC. J Appl Microbiol 80:570–576. https://doi.org/10.1111/j.1365-2672.1996.tb03259.x
Görke B, Stülke J (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6:613–624. https://doi.org/10.1038/nrmicro1932
Groot MN, Klaassens E, de Vos WM, Delcour J, Hols P, Kleerebezem M (2005) Genome-based in silico detection of putative manganese transport systems in Lactobacillus plantarum and their genetic analysis. Microbiology 151:1229–1238. https://doi.org/10.1099/mic.0.27375-0
Güzel-Seydim ZB, Seydim AC, Greene AK, Bodine AB (2000) Determination of organic acids and volatile flavor substances in kefir during fermentation. J Food Compos Anal 13:35–43. https://doi.org/10.1006/jfca.1999.0842
Hayek SA, Gyawali R, Aljaloud SO, Krastanov A, Ibrahim SA (2019) Cultivation media for lactic acid bacteria used in dairy products. J Dairy Res 86:490–502. https://doi.org/10.1017/S002202991900075X
Hickey MW, Hillier AJ, Jago GR (1986) Transport and metabolism of lactose, glucose, and galactose in homofermentative lactobacilli. Appl Environ Microbiol 51:825–831. https://doi.org/10.1128/aem.51.4.825-831.1986
Kaneko T, Takahashi M, Suzuki H (1990) Acetoin fermentation by citrate-positive Lactococcus lactis subsp. lactis 3022 grown aerobically in the presence of hemin or Cu2+. Appl Environ Microbiol 56:2644–2649. https://doi.org/10.1128/aem.56.9.2644-2649.1990
Lavari L, Ianniello R, Páez R, Zotta T, Cuatrin A, Reinheimer J, Parente E, Vinderola G (2015) Growth of Lactobacillus rhamnosus 64 in whey permeate and study of the effect of mild stresses on survival to spray drying. LWT - Food Sci Technol 63:322–330. https://doi.org/10.1016/j.lwt.2015.03.066
Lê NT, Champagne CP, Lee BH, Goulet J (2003) Growth of Lactobacillus paracasei ssp. paracasei on tofu whey. Int J Food Microbiol 89:67–75. https://doi.org/10.1016/S0168-1605(03)00109-0
Le Bars D, Yvon M (2008) Formation of diacetyl and acetoin by Lactococcus lactis via aspartate catabolism. J Appl Microbiol 104:171–177. https://doi.org/10.1111/j.1365-2672.2007.03539.x
Liu S-Q (2003) Practical implications of lactate and pyruvate metabolism by lactic acid bacteria in food and beverage fermentations. Int J Food Microbiol 83:115–131. https://doi.org/10.1016/S0168-1605(02)00366-5
Loizzo MR, Menichini F, Picci N, Puoci F, Spizzirri UG, Restuccia D (2013) Technological aspects and analytical determination of biogenic amines in cheese. Trends Food Sci Technol 30:38–55. https://doi.org/10.1016/j.tifs.2012.11.005
Lu Z, Fleming HP, McFeeters RF (2001) Differential glucose and fructose utilization during cucumber juice fermentation. Food Microbiol Saf 66:162–166. https://doi.org/10.1111/j.1365-2621.2001.tb15600.x
Milesi MM, Wolf IV, Bergamini CV, Hynes ER (2010) Two strains of nonstarter lactobacilli increased the production of flavor compounds in soft cheeses. J Dairy Sci 93:5020–5031. https://doi.org/10.3168/jds.2009-3043
Myers RH, Montgomery DC (2009) Response surface methodology: process and product optimization using designed experiments (Wiley series in probability and statistics). Wiley, New York
Nancib N, Nancib A, Boudjelal A, Benslimane C, Blanchard F, Boudrant J (2001) The effect of supplementation by different nitrogen sources on the production of lactic acid from date juice by Lactobacillus casei subsp. rhamnosus. Bioresour Technol 78:149–153. https://doi.org/10.1016/S0960-8524(01)00009-8
Parente E, Cogan TM, Powel IB (2017) Starter cultures: general aspects. In: McSweeney PLH, Fox PF, Cotter PD, Everett DW (eds) Cheese, chemistry, physics and microbiology, 4th edn. Academic Press, London, pp 201–226
Peralta GH, Wolf IV, Bergamini CV, Perotti MC, Hynes ER (2014) Evaluation of volatile compounds produced by Lactobacillus paracasei I90 in a hard-cooked cheese model using solid-phase microextraction. Dairy Sci Technol 94:73–81. https://doi.org/10.1007/s13594-013-0143-4
Peralta GH, Bergamini CV, Hynes ER (2016a) Aminotransferase and glutamate dehydrogenase activities in lactobacilli and streptococci. Braz J Microbiol 47:741–748. https://doi.org/10.1016/j.bjm.2016.04.005
Peralta GH, Wolf IV, Perotti MC, Bergamini CV, Hynes ER (2016b) Formation of volatile compounds, peptidolysis and carbohydrate fermentation by mesophilic lactobacilli and streptoccocci cultures in a cheese extract. Dairy Sci Technol 96:603–621. https://doi.org/10.1007/s13594-016-0291-4
Peralta GH, Bergamini CV, Audero G, Páez R, Wolf IV, Perotti MC, Hynes ER (2017) Spray-dried adjunct cultures of autochthonous non-starter lactic acid bacteria. Int J Food Microbiol 255:17–24. https://doi.org/10.1016/j.ijfoodmicro.2017.05.014
Pogačić T, Maillard MB, Leclerc A, Hervé C, Chuat V, Valence F, Thierry A (2016) Lactobacillus and Leuconostoc volatilomes in cheese conditions. Appl Microbiol Biotechnol 100:2335–2346. https://doi.org/10.1007/s00253-015-7227-4
Romão BB, da Silva FB, de Resende MM, Cardoso VL (2010) Ethanol production from hydrolyzed soybean molasses. Energy Fuel 26:2310–2316. https://doi.org/10.1021/ef201908j
Roopashri AN, Varadaraj MC (2014) Soy whey based medium for optimized phytase activity in Saccharomyces cerevisiae MTCC 5421 and α-D-galactosidase and antibacterial activities in Lactobacillus plantarum MTCC 5422 by response surface methodology. J Food Sci Technol 51:519–526. https://doi.org/10.1007/s13197-011-0527-5
Stefanovic E, Thierry A, Maillard MB, Bertuzzi A, Rea MC, Fitzgerald G, McAuliffe O, Kilcawley KN (2017) Strains of the Lactobacillus casei group show diverse abilities for the production of flavor compounds in 2 model systems. J Dairy Sci 100:6918–6929. https://doi.org/10.3168/jds.2016-12408
Tamime AY, Skriver A, Nilsson L-E (2006) Starter cultures. In: Tamime A (ed) Fermented milks. Blackwell Science Ltd, Oxford, pp 11–52
Tanous C, Kieronczyk A, Helinck S, Chambellon E, Yvon M (2002) Glutamate dehydrogenase activity: a major criterion for the selection of flavour-producing lactic acid bacteria strains. Antonie Leeuwenhoek 82:271–278. https://doi.org/10.1023/A:1020616506703
Vasiljevic T, Jelen P (2001) Production of β-galactosidase for lactose hydrolysis in milk and dairy products using thermophilic lactic acid bacteria. Innov Food Sci Emerg Technol 2:75–85. https://doi.org/10.1016/S1466-8564(01)00027-3
Vinderola CG, Reinheimer JA (2003) Lactic acid starter and probiotic bacteria: a comparative “in vitro” study of probiotic characteristics and biological barrier resistance. Food Res Int 36:895–904. https://doi.org/10.1016/S0963-9969(03)00098-X
Wang H, Johnson LA, Wang T (2004) Preparation of soy protein concentrate and isolate from extruded-expelled soybean meals. J Am Oil Chem Soc 81:713–717. https://doi.org/10.1007/s11746-004-966-8
Xu GQ, Chu J, Zhuang YP, Wang YH, Zhang SL (2008) Effects of vitamins on the lactic acid biosynthesis of Lactobacillus paracasei NERCB 0401. Biochem Eng J 38:189–197. https://doi.org/10.1016/j.bej.2007.07.003
Zartl B, Silberbauer K, Loeppert R, Viernstein H, Praznik W, Mueller M (2018) Fermentation of non-digestible raffinose family oligosaccharides and galactomannans by probiotics. Food Funct 9:1638–1646. https://doi.org/10.1039/C7FO01887H
Zhong XF, Zhang YB, Huang GD, Ouyang YZ, Liao DJ, Peng JW, Huang WZ (2018) Proteomic analysis of stachyose contribution to the growth of Lactobacillus acidophilus CICC22162. Food Funct 9:2979–2988. https://doi.org/10.1039/C8FO00528A
Zuljan FA, Mortera P, Alarcón SH, Blancato VS, Espariz M, Magni C (2016) Lactic acid bacteria decarboxylation reactions in cheese. Int Dairy J 62:53–62. https://doi.org/10.1016/j.idairyj.2016.07.007
Funding
This work was financed by the Agencia Santafesina de Ciencia, Tecnología e Innovación de la provincia de Santa Fe-ASaCTeI (IO-2017-00036), the Agencia Nacional de Promoción Científica y Tecnológica-ANPCyT (PICT-2018-01334; PICT 2016-0597), and the Universidad Nacional del Litoral-UNL (PIC 50420150100059LI).
Author information
Authors and Affiliations
Contributions
Laboratory work M.V.B. and G.H.P; Optimization design L.V.C.; Volatile compounds determination I.V.W.; Minerals determination R.S.; Writing original draft G.H.P, M.V.B. and C.V.B; Project administration, Conceptualization and Funding acquisition G.H.P; E.R.H.; C.V.B. All authors contributed to writing the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Beret, M.V., Peralta, G.H., Vera-Candioti, L. et al. Culture media based on effluent derived from soy protein concentrate production for Lacticaseibacillus paracasei 90 biomass production: statistical optimisation, mineral characterization, and metabolic activities. Antonie van Leeuwenhoek 114, 2047–2063 (2021). https://doi.org/10.1007/s10482-021-01660-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-021-01660-1