The Evaluation of Activity of Selected Lactic Acid Bacteria for Bioconversion of Milk and Whey from Goat Milk to Release Biomolecules with Antibacterial Activity
Abstract
:1. Introduction
2. Results
2.1. The Comparison of Metabolic Activity
2.2. The Evaluation of Antibacterial Activity
3. Materials and Methods
3.1. Raw Material
3.2. Microbiological Material
3.3. Fermented Milk and Whey Preparation
3.4. Metabolic Activity Analysis
3.5. Antimicrobial Properties Testing
3.5.1. Culture Method in Liquid Medium
3.5.2. Determination of the Reduction in Indicator Microorganisms
3.5.3. Optical Density Measurement Using a Bioscreen C
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Sample Availability
References
- Selvaggi, M.; Laudadio, V.; Dario, C.; Tufarelli, V. Major proteins in goat milk: Updated overview on genetic variability. Mol. Biol. Rep. 2014, 41, 1035–1048. [Google Scholar] [CrossRef] [PubMed]
- Lad, S.S.; Aparnathi, K.D.; Mehta, B.; Velpula, S. Goat milk in human nutrition and health—A review. Int. J. Curr. Microbiol. Appl. Sci. 2017, 5, 1781–1792. [Google Scholar] [CrossRef]
- Clark, S.; Garcia, M.B.A. 100-Year Review: Advances in goat milk research. J. Dairy Sci. 2004, 100, 10026–10044. [Google Scholar] [CrossRef] [PubMed]
- Paulina, G.; Milán, M.J.; Lavín, M.P.; Theodorisis, A.; Morin, E.; Capote, J. Invited review: Current production trends, farm structures and economics of the dairy sheep and goat sectors. J. Dairy Sci. 2018, 101, 6715–6729. [Google Scholar] [CrossRef]
- Picon, A.; Garde, S.; Ávila, M.; Nuñez, M. Microbiota dynamics and lactic acid bacteria biodiversity in raw goat milk cheese. Int. Dairy J. 2016, 58, 14–22. [Google Scholar] [CrossRef]
- Izquierdo-González, J.J.; Amil-Ruiz, F.; Zazzu, S.; Sánchez-Lucas, R.; Fuentes-Almagro, C.A.; Rodríguez-Ortega, M.J. Proteomic analysis of goat milk kefir: Profiling the fermentation-time depensent protein digestion and identification of potential peptides with biological activity. Food Chem. 2019, 295, 456–465. [Google Scholar] [CrossRef]
- Wang, H.; Sun, X.; Song, X.; Guo, M. Effects of kefir grains from different origins on proteolysis and volatile profile of goat milk kefir. Food Chem. 2021, 339, 128099. [Google Scholar] [CrossRef]
- Farnworth, E.R.; Mainville, I. Kefir: A fermented milk product. In Handbook of Fermented Functional Foods; CRC Press: Boca Raton, FL, USA; pp. 94–96.
- Ismaiel, A.A.; Ghaly, M.F.; El-Naggar, A.K. Milk kefir: Ultrastructure, antimicrobial activity and efficacy on aflatoxin B1 production by Aspergillus flavus. Curr. Microbiol. 2011, 62, 1602–1609. [Google Scholar] [CrossRef]
- Garrote, G.L.; Delfederico, L.; Bibiloni, R.; Abraham, A.G.; Perez, P.F.; Semorile, L.; De Antoni, G.L. Lactobacilli isolated from kefir grains: Evidence of the presence of S-layer proteins. J. Dairy Res. 2004, 71, 222–230. [Google Scholar] [CrossRef]
- Güzel-Seydim, Z.B.; Seydim, A.C.; Greene, A.K.; Bodine, A.B. Determination of organic acids and Voltaire flavour substances in kefir during fermentation. J. Food Compos. Anal. 2000, 13, 35–43. [Google Scholar] [CrossRef]
- Costa, M.P.; Conte-Junior, C.A. Chromatographic methods for the determination of carbohydrates and organic acids in food of animal origin. Compr. Rev. Food Sci. Food Saf. 2015, 14, 586–600. [Google Scholar] [CrossRef]
- Frengova, G.I.; Simova, E.D.; Beshkova, D.M.; Simov, Z.I. Exopolysaccharides produced by lactic acid bacteria of kefir grains. Zeitsch Nat. 2002, 57, 805–810. [Google Scholar] [CrossRef] [PubMed]
- Micheli, L.; Uccelletti, D.; Palleschi, C.; Crescenzi, V. Isolation and characterization of a ropy Lactobacillus strain producing the exopolysaccharide kefiran. Appl. Microbiol. Biotechnol. 1999, 53, 69–74. [Google Scholar] [CrossRef] [PubMed]
- Klewicka, E.; Lipińska, L. Aktywność przeciwgrzybowa bakterii fermentacji mlekowej z rodzaju Lactobacillus. Żywność Nauka Technol. Jakość 2016, 1, 17–31. [Google Scholar]
- Reis, J.A.; Paula, T.A.; Casarotti, S.N.; Penna, A.L.B. Lactic acid bacteria antimicrobial compound: Characteristic and application. Food Eng. Rev. 2012, 4, 124–140. [Google Scholar] [CrossRef]
- Paquet, J.; Lacroix, C.; Audet, P.; Thibault, J. Electrical conductivity as a tool for analyzing fermentation processes for production of cheese starters. Int. Dairy J. 2000, 10, 391–399. [Google Scholar] [CrossRef]
- Bougherra, F.; Dilmi-Bouras, A.; Balti, R.; Przybylski, R.; Adoui, A.; Elhameur, H.; Chevalier, M.; Flahaut, C.; Dhulster, P.; Naima, N. Antibacterial activity of new peptide form bovine casein hydrolysed by a serine metalloprotease of Lactococcus lactis subsp. lactis BR16. J. Funct. Foods 2017, 32, 112–122. [Google Scholar] [CrossRef]
- Gut, A.M.; Vasiljevic, T.; Yeager, T.; Donkor, O.N. Kefir characteristics and antibacterial properties—Potential applications in control on enteric bacterial infection. Int. Dairy J. 2021, 118, 105021. [Google Scholar] [CrossRef]
- Miao, J.; Guo YOu, G.; Liu, X.; Fang, Z.; Liao, C.; Ke, Y.; Chen, L.; Zhao, Z.; Cao, Y. Purification and characterization of bacteriocin F1, a novel bacteriocin produced by Lactobacillus paracasei subsp. tolerans FX-6 from Tibetan kefir, a traditional fermented milk from Tibet, China. Food Cont. 2014, 42, 48–53. [Google Scholar]
- Ahmadova, A.; Todorov, S.D.; Hadji-Sfaxi, I.; Choiset, Y.; Rabesona, H.; Messaoudi, S.; Kuliyev, A.; Franco, B.D.; Hobert, J.M.; Haertlé, T. Antimicrobial and antifungal activities of Lactobacillus curvatus strain isolates form homemade Azerbaijani cheese. Anaerobe 2013, 20, 42–49. [Google Scholar] [CrossRef]
- Gheziel, C.; Russo, P.; Pia Arena, M.; Spano, G.; Ouzari, H.; Kheroua, O.; Saidi, D.; Fiocco, D.; Kaddouro, H.; Cappozi, V. Evaluating the Probiotic Potential of Lactobacillus plantarum Strains from Algerian Infant Feces: Towards the Design of Probiotic Starter Cultures Tailored for Developing Countries. Probiotics Antimicrob. Proteins 2019, 11, 113–123. [Google Scholar] [CrossRef] [PubMed]
- Tarrah, A.; Da Silva Duarte, V.; De Castilhos, J.; Pakroo, S.; Junior, W.J.F.L.; Luchese, R.H. Probiotic potential and biofilm inhibitory activity of Lactobacillus casei group strains isolated from infant feces. J. Funct. Foods 2019, 54, 489–497. [Google Scholar] [CrossRef]
- Islam, Z.; Uddin, E.; Rahman, T.; Islam, M.A.; Harun-ur-Rashid, M. Isolation and characterization of dominant lactic acid bacteria from raw goat milk: Assessment of probiotic potential and technological properties. Small Rumin. Res. 2021, 205, 106532. [Google Scholar] [CrossRef]
- Saliba, L.; Zoumpopoulou, G.; Anastosiaou, R.; Hassoun, G.; Karayiannis, Y.; Sgouras, D.; Tsakalidou, E.; Deiana, P.; Montanari, L.; Mangia, N.P. Probiotic and safety assessment of Lactobacillus strains isolated from Lebanese Baladi goat milk. Int. Dairy J. 2021, 120, 105092. [Google Scholar] [CrossRef]
- Lasik, A.; Pikul JMajcher, M.; Lasik-Kurdyś, M.; Konieczny, P. Characteristic of fermented ewe’s milk products with an increased ratio of natural whey proteins to caseins. Small Rumin. Res. 2016, 144, 283–289. [Google Scholar] [CrossRef]
- Biadała, A.; Szablewski, T.; Lasik-Kurdyś, M.; Cegielska-Radziejewska, R. Antimictobial activity of goat’s milk fermented by single strain of kefir grain microflora. Eur. Food Res. Technol. 2020, 246, 1231–1239. [Google Scholar] [CrossRef]
- Appicciafuoco, B.; Dragone, R.; Frazzoli, C.; Bolzoni, G.; Montovani, A.; Ferrini, A. Microbial screening for quinolones residues in cow milk by bio-optical method. J. Pharm. Biomed. Anal. 2015, 106, 179–185. [Google Scholar] [CrossRef]
Lactobacillus plantarum | Lactobacillus fermentum | Lactobacillus rhamnosus | Lactobacillus acidophilus | |
---|---|---|---|---|
Goat milk | 0.9208 B | 0.9335 A | 0.9336 B | 0.9489 B |
Whey from goat milk | 0.8850 A | 0.9652 A | 0.9819 A | 0.8514 A |
Gompertz Equation Coefficients | Dynamic Parameters of Impedance Changes | ||||||
---|---|---|---|---|---|---|---|
a | b | c | r | Imax (ac/e) | x1 (b/c) | Zb ʃf(x)dx | |
Lactobacillus plantarum | 44.12 | 5.10 | 0.48 | 0.99 | 6.79 C**) | 10.63 B | 10.06 C |
Lactobacillus fermentum | 31.51 | 7.38 | 0.66 | 0.94 | 7.65 C | 11.18 C | 7.02 A |
Lactobacillus rhamnosus | 38.15 | 4.25 | 0.37 | 0.97 | 5.19 B | 11.49 C | 8.10 B |
Lactobacillus acidophilus | 45.10 | 2.36 | 0.27 | 0.98 | 4.48 A | 8.74 A | 10.64 C |
Gompertz Equation Coefficients | Dynamic Parameters of Impedance Changes | ||||||
---|---|---|---|---|---|---|---|
a | B | c | r | Imax (ac/e) | x1 (b/c) | Zb ʃf(x)dx | |
Lactobacillus plantarum | 28.64 | 4.44 | 0.40 | 0.99 | 4.21 A**) | 8.11 A | 6.16 B |
Lactobacillus fermentum | 35.19 | 4.11 | 0.39 | 0.96 | 5.05 B | 11.54 B | 7.85 C |
Lactobacillus rhamnosus | 45.09 | 1.92 | 0.22 | 0.95 | 13.65 D | 10.73 B | 10.48 D |
Lactobacillus acidophilus | 21.02 | 3.54 | 0.25 | 0.98 | 11.93 C | 14.16 C | 3.82 A |
Kefir Grain Microflora | Indicator Microorganisms | |||
---|---|---|---|---|
Proteus mirabilis | E. coli | Micrococcus luteus | Salmonella enteritidis | |
Goat milk | ||||
Lactobacillus plantarum | 5:38 | ND | 5:56 | 6:02 |
Lactobacillus fermentum | 5:18 | ND | 5:31 | 5:51 |
Lactobacillus rhamnosus | 5:02 | ND | 5:47 | 5:37 |
Lactobacillus acidophilus | 5:25 | ND | 5:12 | 5:49 |
Whey from goat milk | ||||
Lactobacillus plantarum | 5:58 | ND | 6:22 | 6:34 |
Lactobacillus fermentum | 6:28 | ND | 5:29 | 6:21 |
Lactobacillus rhamnosus | 5:32 | ND | 6:11 | 5:55 |
Lactobacillus acidophilus | 6:35 | ND | 5:38 | 5:59 |
Kefir Grain Microflora | Antimicrobial Activity (Expressed as Late Growth) | |||
---|---|---|---|---|
Proteus mirabilis | E. coli | Micrococcus luteus | Salmonella enteritidis | |
Goat milk | ||||
Lactobacillus plantarum | II | I | 0 | I |
Lactobacillus fermentum | I | I | 0 | 0 |
Lactobacillus rhamnosus | I | II | I | I |
Lactobacillus acidophilus | 0 | I | 0 | I |
Whey from goat milk | ||||
Lactobacillus plantarum | II | II | II | II |
Lactobacillus fermentum | II | II | II | II |
Lactobacillus rhamnosus | 0 | II | I | II |
Lactobacillus acidophilus | II | I | I | I |
Kefir Grain Microflora | Antimicrobial Activity | |||
---|---|---|---|---|
Proteus mirabilis | E. coli | Micrococcus luteus | Salmonella nteritidis | |
Goat milk | ||||
Lactobacillus plantarum | 3.1 × 103 Bc | 1.2 × 105 Ce | NG Aa | 2.1 × 103 Bd |
Lactobacillus fermentum | 1.8 × 102 Bb | 2.6 × 102 Bb | 1NG Aa | NG Aa |
Lactobacillus rhamnosus | 1.6 × 102 Bb | 3.7 × 103 Cc | 1.6 × 102 Bb | NG Aa |
Lactobacillus acidophilus | NG A | 4.3 × 102 Bb | 1.1 × 102 Bb | 1.2 × 102 Bc |
Whey from goat milk | ||||
Lactobacillus plantarum | NG Aa | NG Aa | 2.2 × 102 Bb | 1.3 × 102 Bc |
Lactobacillus fermentum | NG Aa | NG Aa | 2.0 × 102 Cb | 3.8 × 10 Bb |
Lactobacillus rhamnosus | 1.2 × 102 Ab | 1.5 × 104 Cd | 1.2 × 103 Bc | 4.5 × 104 Ce |
Lactobacillus acidophilus | 1 × 103 Cc | 2.6 × 102 Bb | 1.3 × 103 Cc | NG Aa |
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Biadała, A.; Szablewski, T.; Cegielska-Radziejewska, R.; Lasik-Kurdyś, M.; Adzahan, N.M. The Evaluation of Activity of Selected Lactic Acid Bacteria for Bioconversion of Milk and Whey from Goat Milk to Release Biomolecules with Antibacterial Activity. Molecules 2023, 28, 3696. https://doi.org/10.3390/molecules28093696
Biadała A, Szablewski T, Cegielska-Radziejewska R, Lasik-Kurdyś M, Adzahan NM. The Evaluation of Activity of Selected Lactic Acid Bacteria for Bioconversion of Milk and Whey from Goat Milk to Release Biomolecules with Antibacterial Activity. Molecules. 2023; 28(9):3696. https://doi.org/10.3390/molecules28093696
Chicago/Turabian StyleBiadała, Agata, Tomasz Szablewski, Renata Cegielska-Radziejewska, Małgorzata Lasik-Kurdyś, and Noranizan Mohd Adzahan. 2023. "The Evaluation of Activity of Selected Lactic Acid Bacteria for Bioconversion of Milk and Whey from Goat Milk to Release Biomolecules with Antibacterial Activity" Molecules 28, no. 9: 3696. https://doi.org/10.3390/molecules28093696