Abstract
In order to improve cassava’s palatability and reduce its toxicity, this root is fermented and applied in foods, such as sour cassava starch used to prepare cheese bread and biscuits. This fermentation occurs spontaneously with lactic acid bacteria (LAB) and yeasts. However, it remains an empirical process, with long duration and lack of product quality homogeneity. This work aims to use starter cultures in a pilot-scale fermentation process for the production of sour cassava starch. After differentiation of strains, Lactobacillus plantarum Lp3, which exhibited great total titratable acidity (TTA) (5.01 ± 0.05%) and antagonistic activity against Bacillus cereus, Escherichia coli and Salmonella Typhimurium, together with Lactobacillus brevis Lb9 (with lesser TTA values: 2.71 ± 0.10%, but amylolytic activity: 2.75 ± 0.61 mm) were tested as single and co-cultures with Saccharomyces cerevisiae UFMG-A1007. LAB and yeasts were inoculated at counts of 8 and 7 log10 CFU/g, respectively, and they remained until the 28th day only in co-culture, highlighting the importance of the yeast for the LAB viability. Although single cultures lead to higher acidity during fermentation, the final product acidity obtained with single cultures did not differ from the acidity obtained with L. plantarum Lp3 in association with S. cerevisiae UFMG-A1007. Therefore, this co-culture exhibited higher potential to be tested as a starter culture in industrial-scale fermentation studies because both microorganisms were in high counts until the end of fermentation and contributed to a final product safe for human consumption, with satisfactory acidity, expansion capacity, and physicochemical properties.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adebayo CO, Aderiye BI, Akpor OB (2013) Occurrence and antimicrobial properties of lactic acid bacteria during the fermentation of cassava mash, maize and sorghum grains. Microbiol Res Int 1(2):27–32
Albertin W, Marullo P, Aigle M, Dillmann C, Vienne D, Bely M, Sicard D (2011) Population size drives industrial Saccharomyces cerevisiae alcoholic fermentation and is under genetic control. Appl Environ Microbiol 77:2772–2784. https://doi.org/10.1128/AEM.02547-10
Anyogu A, Awamaria B, Sutherland JP, Ouoba LII (2014) Molecular characterisation and antimicrobial activity of bacteria associated with submerged lactic acid cassava fermentation. Food Control 39:119–127. https://doi.org/10.1016/j.foodcont.2013.11.005
AOAC (Association of Official Analytical Chemists) (2016) Official methods of analysis, 20th ed. AOAC International, Gaithersburg. http://www.eoma.aoac.org. Accessed 9 Nov 2016
Botthoulath V, Upaichit A, Thumarat U (2018) Identification and in vitro assessment of potential probiotic characteristics and antibacterial effects of Lactobacillus plantarum subsp. plantarum SKI19, a bacteriocinogenic strain isolated from Thai fermented pork sausage. J Food Sci Technol 55(7):2774–2785. https://doi.org/10.1007/s13197-018-3201-3
Brazil (1978) Decreto nº 12.486, de 20 de outubro de 1978. Aprova normas técnicas especiais relativas a alimentos e bebidas. Diário Oficial do Estado de São Paulo, 3–25
Brazil (2001) Ministério da Saúde. Resolução RDC nº 12, de 02 de janeiro de 2001. Aprova o regulamento técnico sobre os padrões microbiológicos para alimentos. Diário Oficial da União; seção I
Cadena MP, Villarraga EC, Lújan DE, Salcedo JG (2006) Evaluacion de la agroindústria del almidon agrio de yuca (Manihot esculenta Crantz) em Cordoba y Sucre. Temas Agrarios 11(1):43–53. https://doi.org/10.21897/rta.v11i1.639
Cereda MP, Daiuto ER, Vilpoux O (2004) Metodologia de determinação de amido por digestão ácida em microondas. Revista da Associação Brasileira dos Produtores de Amido de Mandioca 2(8):29
De Las Rivas B, Marcobal A, Muñoz R (2006) Development of a multilocus sequence typing method for analysis of Lactobacillus plantarum strains. Microbiol 152:85–93. https://doi.org/10.1099/mic.0.28482-0
Da Silva N, Taniwaki MH, Junqueira VCA, Silveira NFA, Nascimento MS, Gomes RAR (2012) Microbiological examination methods of food and water: a laboratory manual. CRC Press, Boca Raton
De Vuyst L, Camu N, De Winter T, Vandemeulebroecke K, De Perre VV, Vancanneyt M, De Vos P, Cleenwerck I (2008) Validation of the (GTG)5-rep-PCR fingerprinting technique for rapid classification and identification of acetic acid bacteria, with a focus on isolates from Ghanaian fermented cocoa beans. Int J Food Microbiol 125:79–90. https://doi.org/10.1016/j.ijfoodmicro.2007.02.030
Edward VA, Huch M, Dortu C, Thonart P, Egounlety M, Van Zyl PJ, Singh S, Holzapfel WH, Franz CMAP (2011) Biomass production and small-scale testing of freeze-dried lactic acid bacteria starter strains for cassava fermentations. Food Control 22:389–395. https://doi.org/10.1016/j.foodcont.2010.09.008
Food and Agriculture Organization of the United Nations (FAO) (2016) Food outlook: biannual report on global food markets. http://www.fao.org/3/a-i6198e.pdf. Accessed 16 Aug 2018
Food and Agriculture Statistics (FAOSTAT) (2016) http://faostat.fao.org. Accessed 16 Aug 2018
Freire AL, Ramos CL, Almeida EG, Duarte WF, Schwan RF (2014) Study of the physicochemical parameters and spontaneous fermentation during the traditional production of yakupa, an indigenous beverage produced by Brazilian Amerindians. World J Microbiol Biotechnol 30:567–577. https://doi.org/10.1007/s11274-013-1476-0
Freire AL, Ramos CL, Schwan RF (2015) Microbiological and chemical parameters during cassava based-substrate fermentation using potential starter cultures of lactic acid bacteria and yeast. Food Res Int 76:787–795. https://doi.org/10.1016/j.foodres.2015.07.041
Freire AL, Ramos CL, Da Costa Souza PN, Cardoso MG, Schwan RF (2017) Nondairy beverage produced by controlled fermentation with potential probiotic starter cultures of lactic acid bacteria and yeast. Int J Food Microbiol 248:39–46. https://doi.org/10.1016/j.ijfoodmicro.2017.02.011
Gevers D, Huys G, Swings J (2001) Applicability of rep-PCR fingerprinting for identification of Lactobacillus species. FEMS Microbiol Lett 205:31–36. https://doi.org/10.1111/j.1574-6968.2001.tb10921.x
Granza AG, Hornung PS, Zielinski AAF, Nogueira A, Schnitzler E, Demiate IM (2018) Gluten-free baked foods with extended shelf-life. J Food Sci Technol 55(8):3035–3045. https://doi.org/10.1007/s13197-018-3225-8
Houngbédji M, Johansen P, Padonou SW, Akissoé N, Arneborg N, Nielsen DS, Hounhouigan DJ, Jespersen L (2018) Occurrence of lactic acid bacteria and yeasts at species and strain level during spontaneous fermentation of mawè, a cereal dough produced in West Africa. Food Microbiol 76:267–278. https://doi.org/10.1016/j.fm.2018.06.005
Kostinek M, Specht I, Edward VA, Pinto C, Egounlety M, Sossa C, Mbugua S, Dortu C, Thonart P, Taljaard L, Mengu M, Franz CMAP, Holzapfel WH (2007) Characterisation and biochemical properties of predominant lactic acid bacteria from fermenting cassava for selection as starter cultures. Int J Food Microbiol 114:342–351. https://doi.org/10.1016/j.ijfoodmicro.2006.09.029
Lacerda ICA, Miranda RL, Borelli BM, Nunes AC, Nardi RMD, Lachance MA, Rosa CA (2005) Lactic acid bacteria and yeast associated with spontaneous fermentations during the production of sour cassava starch in Brazil. Int J Food Microbiol 105:213–219. https://doi.org/10.1016/j.ijfoodmicro.2005.04.010
Lacerda ICA, Gomes FCO, Borelli BM, Faria CLL Jr, Franco GR, Mourão MM, Morais PB, Rosa CA (2011) Identification of the bacterial community responsible for traditional fermentation during sour cassava starch, cachaça and minas cheese production using culture-independent 16S rRNA gene sequence analysis. Braz J Microbiol 42:650–657. https://doi.org/10.1590/S1517-838220110002000029
Maeda KC, Cereda MP (2001) Avaliação de duas metodologias de expansão ao forno do polvilho azedo. Food Sci Technol 21(2):139–143. https://doi.org/10.1590/S0101-20612001000200003
Marcon MJA, Kurtz DJ, Raguzzoni JC, Delgadillo I, Maraschin M, Soldi V, Reginatto V, Amante ER (2009) Expansion properties of Sour Cassava Starch (Polvilho Azedo): variables related to its practical application in Bakery. Starch 61(12):716–726. https://doi.org/10.1002/star.200900132
Oliveira RBP, Oliveira AL, Glória MBA (2008) Screening of lactic acid bacteria from vacuum packaged beef for antimicrobial activity. Braz J Microbiol 39:368–374. https://doi.org/10.1590/S1517-838220080002000031
Oyewole OB (2001) Characteristics and significance of yeasts’ involvement in cassava fermentation for “fufu” production. Int J Food Microbiol 65:213–218. https://doi.org/10.1016/S0168-1605(01)00431-7
Padonou SW, Nielsen DS, Akissoe NH, Hounhouigan JD, Nago MC, Jakobsen M (2010) Development of starter culture for improved processing of Lafun, an African fermented cassava food product. J Appl Microbiol 109:1402–1410. https://doi.org/10.1111/j.1365-2672.2010.04769.x
Penido FCL, Piló FB, Sandes SHC, Nunes ÁC, Colen G, Oliveira ES, Rosa CA, Lacerda ICA (2018) Selection of starter cultures for the production of sour cassava starch in a pilot-scale fermentation process. Braz J Microbiol 49:823–831. https://doi.org/10.1016/j.bjm.2018.02.001
Querol A, Barrio E (1990) A rapid and simple method for the preparation of yeast mitochondrial DNA. Nucl Acids Res 18(6):1657
Querol A, Barrio E, Ramon D (1992) A comparative study of different methods of yeast strain characterization. Syst Appl Microbiol 15(3):439–446. https://doi.org/10.1016/S0723-2020(11)80219-5
Ramos CL, De Sousa ESO, Ribeiro J, Almeida TMM, Santos CCAA, Abbeg MA, Schwan RF (2015) Microbiological and chemical characteristics of tarubá, an indigenous beverage produced from solid cassava fermentation. Food Microbiol 49:182–188. https://doi.org/10.1016/j.fm.2015.02.005
Reddy G, Altaf M, Naveena BJ, Venkateshwar M, Kumar EV (2008) Amylolytic bacterial lactic acid fermentation—a review. Biotechnol Adv 26:22–34. https://doi.org/10.1016/j.biotechadv.2007.07.004
Schwan RF, Almeida EG, Souza-Dias MAG, Jespersen L (2007) Yeast diversity in rice-cassava fermentations produced by the indigenous Tapirapé people of Brazil. FEMS Yeast Res 7:966–972. https://doi.org/10.1111/j.1567-1364.2007.00241.x
Zhang G, Sun Y, Sadiq FA, Sakandar HA, He G (2018) Evaluation of the effect of Saccharomyces cerevisiae on fermentation characteristics and volatile compounds of sourdough. J Food Sci Technol 55(6):2079–2086. https://doi.org/10.1007/s13197-018-3122-1
Acknowledgements
The Coordination for the Improvement of Higher Education Personnel (CAPES) and the National Council for Scientific and Technological Development (CNPq) (Grant No. MCTI/CNPq-014/2013) financially supported the present work.
Author information
Authors and Affiliations
Corresponding author
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
Penido, F.C.L., de Oliveira Goulart, C., Galvão, Y.C.F. et al. Antagonistic lactic acid bacteria in association with Saccharomyces cerevisiae as starter cultures for standardization of sour cassava starch production. J Food Sci Technol 56, 3969–3979 (2019). https://doi.org/10.1007/s13197-019-03864-w
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13197-019-03864-w