Growth Kinetics of Autochthonous Lactic Acid Bacteria Isolated from Double Cream Cheese as Potential Starter Culture
Abstract
Currently, there is a permanent search for native Lactic Acid Bacteria (LAB) to explore and apply their biodiversity in the development and improvement of industrial processes, with studies of growth kinetics and performance factors being a fundamental tool for biotechnological use. The objective of this study was to determine the kinetic parameters of 12 autochthonous strains (Pediococcus pentosaceus (19), Leuconostoc citreum (20), Pediococcus acidilactici (21), Leuconostoc mesenteroides subsp. Mesenteroides (22, 29), Enterococcus faecium (24, 25), Enterococcus faecalis (27), Weissella viridescens (28), Lactococcus lactis (30), Lacticaseibacillus casei (31) and Limosilactobacillus fermentum (32)) isolated from a traditional Colombian cheese Double Cream Cheese to obtain information that allows establishing the ideal conditions of the inoculum, standardizing the production of metabolites and exploring their use as starter cultures. Fermentation was carried out in UHT milk at 120 rpm and 35-37 °C until stationary phase, and samples were taken over time to determine pH and titratable acidity (TTA). Exponential and logistic models were used to fit the growth kinetics data. Validation of both models was carried out with the coefficient of determination R2, obtaining good consistency for both (R2 = 0.925 - R2 = 0.932), with slight variations in the kinetic parameters in all the strains. The genera Pediococcus, Leuconostoc, Lactococcus, and E. faecium (24) had the shortest adaptation phases (0-2 h), being P. acidilactici (21), Leu. mesenteroides (22), W. viridescens (28), and E. faecium (24) presented the lowest pH values and high acidity percentages, which shows their potential to be included in the native LAB starter culture and for technology and suitability aptitude studies to produce double cream cheese using pasteurized milk without losing the qualities of the original product.
References
O. McAuliffe, "Genetics of Lactic Acid Bacteria", Cheese Academic Press, pp. 227-247, 2017. https://doi.org/10.1016/B978-0-12-417012-4.00009-0
S. Awad, N. Ahmed, and M. El Soda, “Evaluation of isolated starter lactic acid bacteria in Ras cheese ripening and flavour development,” Food Chemistry, vol. 104, no. 3, pp. 1192–1199, 2007. https://doi.org/10.1016/j.foodchem.2007.01.043
I. da Silva Ferrari, J. Viana de Souza, C. Lacerda Ramos, M. Matiuzzi da Costa, R. Freitas Schwan, and F. Silva Dias, “Selection of autochthonous lactic acid bacteria from goat dairies and their addition to evaluate the inhibition of Salmonella typhi in artisanal cheese,” Food Microbiol., vol. 60, pp. 29–38, Dec. 2016. https://doi.org/10.1016/j.fm.2016.06.014
Y. Nami, B. Haghshenas, R. Vaseghi Bakhshayesh, H. Mohammadzadeh Jalaly, H. Lotfi, S. Eslami, M. Amin Hejazi, “Novel autochthonous lactobacilli with probiotic aptitudes as a main starter culture for probiotic fermented milk,” Lwt, vol. 98, pp. 85–93, Dec. 2018 https://doi.org/10.1016/j.lwt.2018.08.035
L. P. Margalho et al., “High throughput screening of technological and biopreservation traits of a large set of wild lactic acid bacteria from Brazilian artisanal cheeses,” Food Microbiology, vol. 100, p. 103872, Dec. 2021. https://doi.org/10.1016/j.fm.2021.103872
P. Oliveira De Souza De Azevedo, “Optimization of the yield of bacteriocin-like substance (BLIS) produced by Pediococcus pentosaceus and its application as food bioconservative,” Doctoral dissertation, Universidade de São Paulo, Sao paulo, 2018.
https://pesquisa.bvsalud.org/gim/resource/en,au:%22Martins%20Neto,%20Viviana%22/biblio-906025
I. De Pasquale, R. Di Cagno, S. Buchin, M. De Angelis, and M. Gobbetti, “Use of autochthonous mesophilic lactic acid bacteria as starter cultures for making Pecorino Crotonese cheese : E ff ect on compositional , microbiological and biochemical attributes,” Food Research International, vol. 116, pp. 1344–1356, Feb. 2019. https://doi.org/10.1016/j.foodres.2018.10.024
F. Rezvani, F. Ardestani, and G. Najafpour, “Growth kinetic models of five species of Lactobacilli and lactose consumption in batch submerged culture,” Brazilian J. Microbiol., vol. 48, no. 2, pp. 251–258, Jan. 2017. https://doi.org/10.1016/j.bjm.2016.12.007
A. Ghimire, A. Kumar Sah, and R. Poudel, “Kinetics and modeling of growth and lactic acid production in Gundruk, a Himalayan fermented vegetable dish,” Food Sci. Nutr., vol. 8, no. 10, pp. 5591-5600, Oct. 2020. https://doi.org/10.1002/fsn3.1854
J. C. Olivares, B. Rua, I. Susaeta and P. Aldamiz-Echevarria, “Growth kinetics of several lactic bacteria useful as starter for ewe’s cheese production,” Biotechnol. Lett., vol. 15, pp. 1071–1076, Oct. 1993. https://doi.org/10.1007/BF00129940
S. Ahmed, F. Ashraf, M. Tariq, and A. Zaidi, “Aggrandizement of fermented cucumber through the action of autochthonous probiotic cum starter strains of Lactiplantibacillus plantarum and Pediococcus pentosaceus,” Ann. Microbiol., vol. 71, no. 33, Aug. 2021. https://doi.org/10.1186/s13213-021-01645-5
K. E. Motato, C. Milani, M. Ventura, F. E. Valencia, P. Ruas-Madiedo, and S. Delgado, “Bacterial diversity of the Colombian fermented milk ‘Suero Costeño’ assessed by culturing and high-throughput sequencing and DGGE analysis of 16S rRNA gene amplicons,” Food Microbiol., vol. 68, pp. 129–136, Dec. 2017. https://doi.org/10.1016/j.fm.2017.07.011
A. F. Londoño-Zapata, M. M. Durango-Zuleta, J. U. Sepúlveda-Valencia, and C. X. Moreno Herrera, “Characterization of lactic acid bacterial communities associated with a traditional Colombian cheese: Double cream cheese,” LWT - Food Sci. Technol., vol. 82, pp. 39–48, Sep. 2017. https://doi.org/10.1016/j.lwt.2017.03.058
M. M. Durango-Zuleta, M. Fuentes-Vanegas, U. Sepúlveda-Valencia, C. Ximena, and M. Herrera, “Isolation, identification, and antimicrobial activity of lactic acid bacteria associated with two traditional Colombian types of cheese: Quesillo and double-cream cheese,” LWT, vol. 171, p. 114119, Dec. 2022. https://doi.org/10.1016/j.lwt.2022.114119
The Association of Official Analytical Chemists, "Official Methods of Analysis," AOAC international, 17th Edition, Gaithersburg, Maryland, USA, 2000.
P. Doran, "Bioprocess Engineering Principles". Elsevier, 2nd Edition, 2012. https://www.elsevier.com/books/bioprocess-engineering-principles/doran/978-0-08-091770-2#
S. M. Mustafa, L. S. Chua, H. A. El-Enshasy, F. A. Abd Majid, and S. Z. Hanapi, “Kinetic profile and anti-diabetic potential of fermented Punica granatum juice using Lactobacillus casei,” Process Biochem., vol. 92, pp. 224–231, May. 2020. https://doi.org/10.1016/j.procbio.2020.01.014
A. Z. Andersen, A. L. Carvalho, A. R. Neves, H. Santos, U. Kummer, and L. F. Olsen, “The metabolic pH response in Lactococcus lactis: An integrative experimental and modelling approach,” Comput. Biol. Chem., vol. 33, no. 1, pp. 71–83, Feb. 2009. https://doi.org/10.1016/j.compbiolchem.2008.08.001
P. G. Hamill et al., “Microbial lag phase can be indicative of, or independent from, cellular stress,” Sci. Reports, vol. 10, no. 5948, Apr. 2020. https://doi.org/10.1038/s41598-020-62552-4
S. Jeanson et al., “Milk acidification by Lactococcus lactis is improved by decreasing the level of dissolved oxygen rather than decreasing redox potential in the milk prior to inoculation,” Int. J. Food Microbiol., vol. 131, no. 1, pp. 75–81, Apr. 2009. https://doi.org/10.1016/j.ijfoodmicro.2008.09.020
F. E. Valencia-García, K. E. Motato-Rocha, M. Y. Vera-Peña, and M. L. Sepúlveda-Lindarte, “Kinetic parameters of lactic acid bacterial isolated from fermented milk ‘suero costeño,’” DYNA, vol. 85, no. 206, pp. 155–161, Jul. 2018. https://doi.org/10.15446/dyna.v85n206.70995
Y. Demarigny, "Lactococcus: Lactococcus lactis Subspecies lactis and cremoris", Encyclopedia of Food Microbiology, Second Edition, Elsevier, 2014, pp. 442-446. https://doi.org/10.1016/B978-0-12-384730-0.00182-8
Y. García-Hernández, T. Pérez-sánchez, Y. García-curbelo, D. Sosa-cossio, and J. R. Nicoli, “Growth ability, microbial activity and susceptibility to antimicrobials of two strains of Pediococcus pentosaceus, candidates to probiotic” Cuba. J. Agric. Sci., vol. 51, no. 4, pp. 433–442, 2017. http://scielo.sld.cu/scielo.php?script=sci_abstract&pid=S2079-34802017000400433&lng=es&nrm=iso&tlng=en
D. Hu et al., “Evaluation of Pediococcus pentosaceus strains as probiotic adjunct cultures for soybean milk post-fermentation,” Food Res. Int., vol. 148, p. 110570, Oct. 2021. https://doi.org/10.1016/j.foodres.2021.110570
S. T. Sarhir, R. Belkhou, A. Bouseta, and A. A. Hayaloglu, “Evaluation of Techno-Functional and Biochemical Characteristics of Selected Lactic Acid Bacteria (Lactococcus Lactis And Leuconostoc Mesenteroides) Used for the Production of Moroccan Fermented Milk, Lben,” SSRN, Jun. 2022. https://doi.org/10.2139/ssrn.4128808
E. H. Drosinos, M. Mataragas, and J. Metaxopoulos, “Modeling of growth and bacteriocin production by Leuconostoc mesenteroides E131,” Meat Sci., vol. 74, no. 4, pp. 690–696, Dec. 2006. https://doi.org/10.1016/j.meatsci.2006.05.022
G. Zurera-Cosano, R. M. García-Gimeno, R. Rodríguez-Pérez, and C. Hervás-Martínez, “Performance of response surface model for prediction of Leuconostoc mesenteroides growth parameters under different experimental conditions,” Food Control, vol. 17, no. 6, pp. 429–438, Jun. 2006. https://doi.org/10.1016/j.foodcont.2005.02.003
Y. Widyastuti, A. Febrisiantosa, and F. Tidona, “Health-Promoting Properties of Lactobacilli in Fermented Dairy Products,” Front. Microbiol., vol. 12, May 2021. https://doi.org/10.3389/fmicb.2021.673890
M. M. Alvarez, E. J. Aguirre-Ezkauriatza, A. Ramírez-Medrano, and Á. Rodríguez-Sánchez, “Kinetic analysis and mathematical modeling of growth and lactic acid production of Lactobacillus casei var. rhamnosus in milk whey,” J. Dairy Sci., vol. 93, no. 12, pp. 5552–5560, Dec. 2010. https://doi.org/10.3168/jds.2010-3116
E. Ghalouni, O. Hassaine, and N. Karam, “Phenotypic Identification and Technological Characterization of Lactic Acid Bacteria Isolated from L ’ ben , An Algerian Traditional Fermented Cow Milk,” J. Pure Appl. Microbiol., vol. 12, no.2, 2018. http://dx.doi.org/10.22207/JPAM.12.2.11
P. Sarantinopoulos, L. Makras, F. Vaningelgem, G. Kalantzopoulos, L. De Vuyst, and E. Tsakalidou, “Growth and energy generation by Enterococcus faecium FAIR-E 198 during citrate metabolism,” Int. J. Food Microbiol., vol. 84, no. 2, pp. 197–206, Jul. 2003. https://doi.org/10.1016/S0168-1605(02)00421-X
H. Choi, Y. W. Kim, I. Hwang, J. Kim, and S. Yoon, “Evaluation of Leuconostoc citreum HO12 and Weissella koreensis HO20 isolated from kimchi as a starter culture for whole wheat sourdough,” Food Chem., vol. 134, no. 4, pp. 2208–2216, Oct. 2012. https://doi.org/10.1016/j.foodchem.2012.04.047
H. Araújo-Rodrigues et al., “Technological and protective performance of LAB isolated from Serpa PDO cheese: Towards selection and development of an autochthonous starter culture,” Lwt, vol. 150, p. 112079, Oct. 2021. https://doi.org/10.1016/j.lwt.2021.112079
L. González, A. Fernández Cuadrillero, J. M. Castro, A. Bernardo, and M. E. Tornadijo, “Selection of Lactic Acid Bacteria Isolated from San Simon da Costa Cheese (PDO) in Order to Develop an Autochthonous Starter Culture,” Adv. Microbiol., vol. 05, no. 11, pp. 748–759, Oct. 2015. https://doi.org/10.4236/aim.2015.511079
A. Monteagudo-Mera, I. Caro, L. B. Rodriguez-Aparicio, J. Rua, M. A. Ferrero, and M. R. Garcia-Armesto, “Characterization of certain bacterial strains for potential use as starter or probiotic cultures in dairy products,” J. Food Prot., vol. 74, no. 8, pp. 1379–1386, Aug. 2011. https://europepmc.org/article/MED/21819671
S. Abbasiliasi et al., “In vitro assessment of Pediococcus acidilactici Kp10 for its potential use in the food industry,” BMC Microbiol., vol. 17, no. 121, May. 2017. https://doi.org/10.1186/s12866-017-1000-z
A. Terzić-Vidojević, K. Veljović, N. Popović, M. Tolinački, and N. Golić, “Enterococci from Raw-Milk Cheeses: Current Knowledge on Safety, Technological, and Probiotic Concerns,” Foods, vol. 10, no. 11, Nov. 2021. https://doi.org/10.3390/foods10112753
E. Zubaidah, I. Susanti, S. S. Yuwono, A. P. Rahayu, I. Srianta, and P. J. Blanc, “Effect of lactobacillus plantarum and leuconostoc mesenteroides starter cultures in lower salt concentration fermentation on the sauerkraut quality,” Food Res., vol. 4, no. 4, pp. 1038–1044, Aug. 2020. https://doi.org/10.26656/fr.2017.4(4).029
B. Kunduhoglu, O. Elcioglu, Y. Gezginc, I. Akyol, S. Pilatin, and A. Cetinkaya, “Genotypic identification and technological characterization of lactic acid bacteria isolated from traditional Turkish Kargi tulum cheese,” African J. Biotechnol., vol. 11, no. 28, pp. 7218–7226, Mar. 2014. https://www.ajol.info/index.php/ajb/article/view/102265
S. Abid et al., “Identification, Biochemical Characterization, and Safety Attributes of Locally Isolated Lactobacillus fermentum from Bubalus bubalis (buffalo) Milk as a Probiotic,” Microorganisms, vol. 10, no. 5, p. 954, Apr. 2022. https://doi.org/10.3390/microorganisms10050954
J. Yang et al., “Selection of functional lactic acid bacteria as starter cultures for the fermentation of Korean leek (Allium tuberosum Rottler ex Sprengel.),” Int. J. Food Microbiol., vol. 191, pp. 164–171, Nov. 2014. https://doi.org/10.1016/j.ijfoodmicro.2014.09.016
I. Carafa et al., “Evaluation of autochthonous lactic acid bacteria as starter and non-starter cultures for the production of Traditional Mountain cheese,” Food Res. Int., vol. 115, pp. 209–218, Jan. 2019. https://doi.org/10.1016/j.foodres.2018.08.069
S. Delgado, A. M. O. Leite, P. Ruas-Madiedo, and B. Mayo, “Probiotic and technological properties of Lactobacillus spp. Strains from the human stomach in the search for potential candidates against gastric microbial dysbiosis,” Front. Microbiol., vol. 5, no. 766, Jan. 2015. https://doi.org/10.3389/fmicb.2014.00766
K. Zarour, A. Prieto, A. Pérez-Ramos, M. Kihal, and P. López, “Analysis of technological and probiotic properties of Algerian L. mesenteroides strains isolated from dairy and non-dairy products,” J. Funct. Foods, vol. 49, pp. 351–361, Oct. 2018. https://doi.org/10.1016/j.jff.2018.09.001
A Endo, S. Maeno, and S. Q. Liu,"Lactic acid bacteria: Leuconostoc spp.," Encyclopedia of Dairy Sciences, Third edition, Elsevier, 2021, pp. 226-232. https://kyushu-u.elsevierpure.com/en/publications/lactic-acid-bacteria-leuconostoc-spp
E. Abedi and S. M. B. Hashemi, “Lactic acid production – producing microorganisms and substrates sources-state of art,” Heliyon, vol. 6, no. 10, p. e04974, Oct. 2020. https://doi.org/10.1016/j.heliyon.2020.e04974
Y. Tuncer, “Some technological properties of phenotypically identified enterococci strains isolated from Turkish tulum cheese,” African J. Biotechnol., vol. 8, no. 24, pp. 7008-7016, Dec. 2009. https://www.researchgate.net/publication/228631661_Some_technological_properties_of_phenotypically_identified_enterococci_strains_isolated_from_Turkish_Tulum_cheese
A. A. Soro-Yao, S. Aka, P. Thonart, and K. M. Djè, “Assessment of the Potential of Lactic Acid Bacteria as Dried Starter Culture for Cereal Fermentation,” Open Biotechnol. J., vol. 8, Feb. 2014. https://doi.org/10.2174/1874070701408010001
H. Peace Uwamahoro, F. Li, A. Timilsina, B. Liu, X. Wang, and Y. Tian, “An Assessment of the Lactic Acid-Producing Potential of Bacterial Strains Isolated from Food Waste,” microbiology research, vol. 13, no. 2, pp. 278-291, May. 2022. https://doi.org/10.3390/microbiolres13020022
K. Śliżewska and A. Chlebicz-Wójcik, “Growth Kinetics of Probiotic Lactobacillus Strains in the Alternative, Cost-Efficient Semi-Solid Fermentation Medium,” Biology, vol. 9, no. 12, p. 423, Nov. 2020. https://doi.org/10.3390/biology9120423
J. I. Ramirez-Pérez et al., “Effect of linear and branched fructans on growth and probiotic characteristics of seven Lactobacillus spp . isolated from an autochthonous beverage from Chiapas , Mexico,” Arch. Microbiol., vol. 204, no. 364, Jun. 2022. https://doi.org/10.1007/s00203-022-02984-w
W. Qiao et al., “Genomic Features and Construction of Streamlined Genome Chassis of Nisin Z Producer Lactococcus lactis N8,” microorganisms, vol. 10, no. 1, p. 47, Dec. 2021. https://doi.org/10.3390/microorganisms10010047
P. F. Weng, Z. F. Wu, and L. L. Lei, “Predictive models for growth of leuconostoc citreum and its dynamics in pickled vegetables with low salinity,” J. Food Process Eng., vol. 36, no. 3, pp. 284–291, Aug. 2012. https://doi.org/10.1111/j.1745-4530.2012.00690.x
C. Mendoza-avendaño et al., “Evaluation of bioactive and anti-nutritional compounds during soymilk fermentation with lactobacillus plantarum bal-03-ittg and Lactobacillus fermentum BAL-21-ITTG,” Rev. Mex. Ing. Quim., vol. 18, no. 3, pp. 967-978, Jan. 2019. https://doi.org/10.24275/uam/izt/dcbi/revmexingquim/2019v18n3/Mendoza
I. Caro et al., “Characterization of Lactococcus strains isolated from artisanal Oaxaca cheese,” LWT, vol. 122, p. 109041, Mar. 2020. https://doi.org/10.1016/j.lwt.2020.109041
S. D. Todorov, C. M. Dioso, M. T. Liong, L. A. Nero, K. Khosravi-Darani, and I. V. Ivanova, “Beneficial features of pediococcus: from starter cultures and inhibitory activities to probiotic benefits,” World J. Microbiol. Biotechnol., vol. 39, no. 4, Nov. 2022. https://doi.org/10.1007/s11274-022-03419-w
C. G. Teixeira, R. R. da Silva, A. Fusieger, E. Martins, R. de Freitas, and A. F. de Carvalho, “The Weissella genus in the food industry: A review,” Res. Soc. Dev., vol. 10, no. 5, p. e8310514557, Apr. 2021. https://doi.org/10.33448/rsd-v10i5.14557
P. Dolci et al., “Impact of Lactococcus lactis as starter culture on microbiota and metabolome profile of an Italian raw milk cheese,” Int. Dairy J., vol. 110, p. 104804, Nov. 2020. https://doi.org/10.1016/j.idairyj.2020.104804
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