Overproduction of gamma-aminobutyric acid and increased antioxidant capacity by Lactiplantibacillus pentosus TEJ4 through optimization by response surface methodology
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Keywords

Bioactive compounds
Draper-Lin small composite design
DPPH
GABA
lactic acid bacteria Bacterias ácido lácticas
compuestos bioactivos
diseño compuesto reducido de Draper-Lin
DPPH
GABA

How to Cite

Orantes-Pérez, D. O., Vázquez-Ovando, A., Coronel-Niño, R., López-Martínez, G., Ruiz-González, S., & Mejía-Reyes, D. (2024). Overproduction of gamma-aminobutyric acid and increased antioxidant capacity by Lactiplantibacillus pentosus TEJ4 through optimization by response surface methodology. Revista Colombiana De Investigaciones Agroindustriales, 11(2), 48–63. https://doi.org/10.23850/24220582.6398

Abstract

Lactic Acid bacteria (LAB) are the main producers of bioactive compounds (peptides, exopolysaccharides, antioxidant compounds, gamma-aminobutyric acid-GABA, etc.). Different strains produce at least one metabolite in high quantities as part of their metabolism, however, there are few reports of LAB with the capacity to produce two or more metabolites simultaneously. Due, the ability of 35 LAB strains previously isolated from dairy products, fermented beverages, and honey to produce gamma-aminobutyric acid (GABA) and the antioxidant capacity was determined. Based on analysis of variance and subsequent comparison of means, the Lactiplantibacillus pentosus strain was selected, and subsequently, using a Draper-Lin small composite design, the conditions of the culture medium (MRS broth) were optimized to achieve the highest production of GABA and increase the antioxidant capacity evaluated by the DPPH assay. The optimal conditions for obtaining 7.99 mg/mL of GABA were 100 mM glutamic acid, a pH of 6, a temperature of 40 °C, and 72 h of fermentation. To obtain the highest antioxidant capacity (6.87 µmol TE/mL), 200 mM glutamic acid and a pH of 4.0 were used. We reported an isolated strain of nondairy product (L. pentosus TEJ4) with the capacity to produce both bioactive, GABA, and antioxidants in a single fermentation process in a non-dairy defined medium, which is a feasible alternative to the normal process of producing bioactive compounds.

https://doi.org/10.23850/24220582.6398
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References

Barrios-Roblero, C., Rosas-Quijano, R., Salvador-Figueroa, M., Gálvez-López, D., & Vázquez-Ovando, A. (2019). Antifungal lactic acid bacteria isolated from fermented beverages with activity against Colletotrichum gloeosporioides. Food Bioscience, 29, 47-54. https://doi.org/10.1016/j.fbio.2019.03.008

Budiari, S., Maryati, Y., Susilowati, A., Mulyani, H., & Lotulung, P. (2019). The effect of lactic acid fermentation in antioxidant activity and total polyphenol contents of the banana (Musa acuminate Linn) juice. AIP Conference Proceedings, 2175, 020024. https://doi.org/10.1063/1.5134588

Chen, H. Y., Hsieh, C. W., Chen, P. C., Lin, S. P., Lin, Y. F., & Chen K. C. (2021). Development and optimization of djulis sourdough bread fermented by lactic acid bacteria for antioxidant capacity. Molecules, 26, 5658. https://doi.org/10.3390/molecules26185658

Cobo-Monterroza, R., Rosas-Quijano, R., Gálvez-López, D., Adriano-Anaya, L., & Vázquez-Ovando, A. (2019). Native lactic acid bacteria as a starter culture for the production of Mexican cream cheese. Agronomía Mesoamericana, 30, 855-870. https://doi.org/10.15517/am.v30i3.34673

Cui, Y., Miao, K., Niyaphorn, S., & Qu, X. (2020). Production of gamma-aminobutyric acid from lactic acid bacteria: A systematic review. International Journal of Molecular Science, 21, 995. https://doi.org/10.3390/ijms21030995

Devi, P. B., Rajapuram, D. R., Jayamanohar, J., Verma, M., Kavitake, D., Avany, B. A. M., Rani, P. U., Ravi, R., & Shetty, P. H. (2023). Gamma-aminobutyric acid (GABA) production by potential probiotic strains of indigenous fermented foods origin and RSM based production optimization. LWT, 176, 114511. https://doi.org/10.1016/j.lwt.2023.114511

Ding, W., Wang, L., Zhang, J., Ke, W., Zhou, J., Zhu, J., Guo, X., & Long, R. (2017). Characterization of antioxidant properties of lactic acid bacteria isolated from spontaneously fermented yak milk in the Tibetan Plateau. Journal of Functional Foods, 35, 481-488. https://doi.org/10.1016/j.jff.2017.06.008

Domínguez-Hernández, C. R., García-Alvarado, M. A., García-Galindo, H. S., Salgado-Cervantes, M. A., & Beristain, C. I. (2016). Stability, antioxidant capacity and bioavailability of nano-emulsified astaxanthin. Revista Mexicana de Ingeniería Química, 15, 457-468. https://www.redalyc.org/articulo.oa?id=62046829013

Drakula, S., Novotni, D., Mustač, N. Č., Voučko, B., Krpan, M., Hruškar, M., & Ćurić, D. (2021). Alteration of phenolics and antioxidant capacity of gluten-free bread by yellow pea flour addition and sourdough fermentation. Food Bioscience, 44, 101424. https://doi.org/10.1016/j.fbio.2021.101424

Edalatian-Dovom, M. R., Habibi-Najafi, M. B., Rahnama-Vosough, P., Norouzi, N., Ebadi-Nezhad, S. J., & Mayo, B. (2023). Screening of lactic acid bacteria strains isolated from Iranian traditional dairy products for GABA production and optimization by response surface methodology. Scientific Reports, 13, 440. https://doi.org/10.1038/s41598-023-27658-5

Fan, X., Yu, L., Shi, Z., Li, C., Zeng, X., Wu, Z., & Pan, D. (2023). Characterization of a novel flavored yogurt enriched in γ-aminobutyric acid fermented by Levilactobacillus brevis CGMCC1. 5954. Journal of Dairy Science, 106, 852-867. https://doi.org/10.3168/jds.2022-22590

Fernández-Roblero, S., Vázquez-Ovando, A., Grajales-Conesa, J., Rincón-Rabanales, M., & Coronel-Niño, R. (2020). Lactic acid bacteria isolated from the Stingless bee Scaptotrigona mexicana and partial characterization of their probiotic activity. BioCiencias, 7, Article 17. https://doi.org/10.15741/revbio.07.e979

Gali, V., Venturi, M., Mari, E., Guerrini, S., & Granchi, L. (2022). Gamma-aminobutyric acid (GABA) production in fermented milk by lactic acid bacteria isolated from spontaneous raw milk fermentation. International Dairy Journal, 127, 105284. https://doi.org/10.1016/j.idairyj.2021.105284

Gálvez-Medina, A. (2020). Capacidad antagónica de bacterias ácido lácticas contra patógenos contaminantes del queso fresco [Tesis de licenciatura, Universidad Autónoma de Chiapas, México].

Ghazanfari, N., Fallah, S., Vasiee, A., & Yazdi, F. T. (2023). Optimization of fermentation culture medium containing food waste for l-glutamate production using native lactic acid bacteria and comparison with industrial strain. LWT, 184, 114871. https://doi.org/10.1016/j.lwt.2023.114871

Ghiasi, F., Hashemi, S. M. B., & Abedi, E. (2023). Effective enhancement of food oxidative stability induced by Lactobacillus strains: In vitro activity. Food Control, 153, 109912. https://doi.org/10.1016/j.foodcont.2023.109912

Gonzalez-Gonzalez, C. R., Machado, J., Correia, S., McCartney, A. L., Stephen-Elmore, J., & Jauregui, P. (2019). Highly proteolytic bacteria from semi-ripened Chiapas cheese elicit angiotensin-I converting enzyme inhibition and antioxidant activity. LWT, 111, 449-456. https://doi.org/10.1016/j.lwt.2019.05.039

Huang, Y., Su, L., & Wu, J. (2016). Pyridoxine supplementation improves the activity of recombinant glutamate decarboxylase and the enzymatic production of gamma-aminobutyric acid. PLoS One, 11, e0157466. https://doi.org/10.1371/journal.pone.0157466

Hur, S. J., Lee, S. Y., Kim, Y. C., Choi, I., & Kim, G. B. (2014). Effect of fermentation on the antioxidant activity in plant-based foods. Food Chemistry, 160, 346-356. https://doi.org/10.1016/j.foodchem.2014.03.112

Jitpakdee, J., Kantachote, D., Kanzaki, H., & Nitoda, T. (2021). Selected probiotic lactic acid bacteria isolated from fermented foods for functional milk production: Lower cholesterol with more beneficial compounds. LWT, 135, 110061. https://doi.org/10.1016/j.lwt.2020.110061

Kanklai, J., Somwong, T. C., Rungsirivanich, P., & Thongwai, N. (2020). Screening of GABA-producing lactic acid bacteria from Thai fermented foods and probiotic potential of Levilactobacillus brevis F064A for GABA-fermented mulberry juice production. Microorganisms, 9, 33. https://doi.org/10.3390/microorganisms9010033

Kuerban, D., Lu, J., Huangfu, Z., Wang, L., Qin, Y., & Zhang, M. (2023). Optimization of fermentation conditions and metabolite profiling of grape juice fermented with lactic acid bacteria for improved flavor and bioactivity. Foods, 12, 2407. https://doi.org/10.3390/foods12122407

Kuo, H. C., Kwong, H. K., Chen, H. Y., Hsu, H. Y., Yu, S. H., Hsieh, C. W., Lin, H. W., Chu, Y. L., & Cheng, K. C. (2021). Enhanced antioxidant activity of Chenopodium formosanum Koidz. by lactic acid bacteria: Optimization of fermentation conditions. PLoS One, 16, e0249250. https://doi.org/10.1371/journal.pone.0249250

Łepecka, A., Szymański, P., Okoń, A., & Zielińska, D. (2023). Antioxidant activity of environmental lactic acid bacteria strains isolated from organic raw fermented meat products. LWT, 174, 114440. https://doi.org/10.1016/j.lwt.2023.114440

Li, H., Li, B., Gao, L., Ge, R., Cui, X., Zhou, J., & Li, Z. (2023). Gamma-aminobutyric acid (GABA) promotes characteristics of Levilactobacillus sp. LB-2. LWT, 184, 115014. https://doi.org/10.1016/j.lwt.2023.115014

López-Rojo, J. P., García-Pinilla, S., Hernández-Sánchez, H., & Cornejo-Mazón, M. (2017). Estudio de la fermentación de kéfir de agua de piña con tibicos. Revista Mexicana de Ingeniería Química, 16, 405-414. https://www.redalyc.org/articulo.oa?id=62052087007

Luscher, B., Maguire, J. L., Rudolph, U., & Sibille, E. (2023). GABAA receptors as targets for treating affective and cognitive symptoms of depression. Trends in Pharmacological Sciences, 44, 586-600. https://doi.org/10.1016/j.tips.2023.06.009

Madrigales-Reátiga, L. F., Castro-Montoya, Y. A., Reyes-Moreno, C., Gutiérrez-Dorado, R., Salas-López, F., Perales-Sánchez, J. X. K. (2024). Chia seed germination and extrusion to increase nutritional value, phenolic compounds, GABA, antioxidant activity, and in vitro antihypertensive potential. Agrociencia, Early Access (58-4). https://doi.org/10.47163/agrociencia.v58i4.3043

Mıdık, F., Tokatlı, M., Bağder Elmacı, S., & Özçelik, F. (2020). Influence of different culture conditions on exopolysaccharide production by indigenous lactic acid bacteria isolated from pickles. Archives of Microbiology, 202, 875-885. https://doi.org/10.1007/s00203-019-01799-6

Morales-Nolasco, E., Adriano-Anaya, L., Gálvez-López, D., Rosas-Quijano, R., & Vázquez-Ovando, A. (2020). Physicochemical, sensory, and microbiological characteristics of ‘queso crema’ cheese made with lactic acid bacteria as a starter culture. Biotecnia, 22, 34-36. https://doi.org/10.18633/biotecnia.v22i1.1129

Myers, R. H., Montgomery, D. C., & Anderson-Cook, C. M. (2009). Response Surface Methodology. Process and product optimization using designed experiments. 3rd ed. Wiley.

Nikolaidis, M. G., & Margaritelis, N. V. (2023). Free radicals and antioxidants: appealing to magic. Trends in Endocrinology & Metabolism, 34, 503-504. https://doi.org/10.1016/j.tem.2023.06.001

Pannerchelvan, S., Rios-Solis, L., Faizal-Wong, F. W., Zaidan, U. H., Wasoh, H., Mohamed, M. S., Tan, J. S., Mohamad, R., & Halim, M. (2023). Strategies for improvement of gamma-aminobutyric acid (GABA) biosynthesis via lactic acid bacteria (LAB) fermentation. Food & Function, 14, 3929-3948. https://doi.org/10.1039/D2FO03936B

Park, S. J., Kim, D. H., Kang, H. J., Shin, M., Yang, S. Y., Yang, J., & Jung, Y. H. (2021). Enhanced production of γ-aminobutyric acid (GABA) using Lactobacillus plantarum EJ2014 with simple medium composition. LWT, 137, 110443. https://doi.org/10.1016/j.lwt.2020.110443

Qadi, W. S., Mediani, A., Kasim, Z. M., Misnan, N. M., Sani, N. A., & Jamar, N. H. (2023). Biological characterization and metabolic variations among cell-free supernatants produced by selected plant-based lactic acid bacteria. Metabolites, 13, 849. https://doi.org/10.3390/metabo13070849

Raethong, N., Santivarangkna, C., Visessanguan, W., Santiyanont, P., Mhuantong, W., & Chokesajjawatee, N. (2022). Whole-genome sequence analysis for evaluating the safety and probiotic potential of Lactiplantibacillus pentosus 9D3, a gamma-aminobutyric acid (GABA)-producing strain isolated from Thai pickled weed. Frontiers in Microbiology, 13, 969548. https://doi.org/10.3389/fmicb.2022.969548

Rafati, H., Talebpour, Z., Adlnasab, L., & Ebrahimi, S. N. (2009). Quality by design: Optimization of a liquid filled pH-responsive macroparticles using Draper-Lin composite design. Journal of Pharmaceutical Sciences, 98(7), 2401-2411. https://doi.org/10.1002/jps.21625

Sahab-Novia, R. M., Suboto, E., Balia-Roostita, L., & Utama-Gemilang, L. (2020). γ-aminobutyric acid found in fermented foods and beverages: Current trends. Heliyon, 6, e05526. https://doi.org/10.1016/j.heliyon.2020.e05526

Santos-Espinosa, A., Beltrán-Barrientos, L. M., Reyes-Díaz, R., Mazorra-Manzano, M. A., Hernández-Mendoza, A., González-Aguilar, G. A., Sáyago-Ayerdi, S. G., Vallejo-Cordoba, B., & González-Córdova, A. F. (2020). Gamma-aminobutyric acid (GABA) production in milk fermented by specific wild lactic acid bacteria strains isolated from artisanal Mexican cheeses. Annals of Microbiology, 70, 12. https://doi.org/10.1186/s13213-020-01542-3

Song, H. Y., & Yu, R.C. (2018). Optimization of culture conditions for gamma-aminobutyric acid production in fermented adzuki bean milk. Journal of Food Drug Analysis, 26, 74-81. https://doi.org/10.1016/j.jfda.2016.11.024

Tan, X., Zhang, S., Liu, J., Xiang, W., Zhang, Q., & Tang, J. (2024). Effect of Lactiplantibacillus plantarum cell-free supernatant on the physiology, quorum sensing, transcription, and enhanced GABA production of Enterococcus faecium. LWT, 198, 115986. https://doi.org/10.1016/j.lwt.2024.115986

Tanamool, V., Hongsachart, P., & Soemphol, W. (2019). Screening and characterisation of gamma-aminobutyric acid (GABA) producing lactic acid bacteria isolated from Thai fermented fish (Plaa-som) in Nong Khai and its application in Thai fermented vegetables (Som-pak). Food Science and Technology, 40, 483-490. https://doi.org/10.1590/fst.05419

Vidal-Gutiérrez, M., Robles-Zepeda, R. E., Vilegas, W., Gonzalez-Aguilar, G. A., Torres-Moreno, H., & López-Romero, J. C. (2020). Phenolic composition and antioxidant activity of Bursera microphylla A. Gray. Industrial Crops and Products, 152, 112412. https://doi.org/10.1016/j.indcrop.2020.112412

Wang, S., Amigo-Benavent, M., Mateos, R., Bravo, L., & Sarriá, B. (2017). Effects of in vitro digestion and storage on the phenolic content and antioxidant capacity of a red grape pomace. International Journal of Food Sciences and Nutrition, 68, 188-200. https://doi.org/10.1080/09637486.2016.1228099

Wei, L., Li, Y., Hao, Z., Zheng, Z., Yang, H., Xu, S., Li, S., Zhang, L., & Xu, Y. (2023). Fermentation improves antioxidant capacity and γ-aminobutyric acid content of Ganmai Dazao Decoction by lactic acid bacteria. Frontiers in Microbiology, 14,1274353. https://doi.org/10.3389/fmicb.2023.1274353

Woraratphoka, J., Innok, S., Soisungnoen, P., Tanamool, V., & Soemphol, W. (2022). γ-Aminobutyric acid production and antioxidant activities in fresh cheese by Lactobacillus plantarum L10-11. Food Science and Technology, 42, e03121. https://doi.org/10.1590/fst.03121

Xu, N., Wei, L., & Liu, J. (2017). Biotechnological advances and perspectives of gamma-aminobutyric acid production. World Journal of Microbiology and Biotechnology, 33, 1-11. https://doi.org/10.1007/s11274-017-2234-5

Yogeswara, I. B. A., Maneerat, S., & Haltrich, D. (2020). Glutamate decarboxylase from lactic acid bacteria—A key enzyme in GABA synthesis. Microorganisms, 8, 1923. https://doi.org/10.3390/microorganisms8121923

Zareian, M., Ebrahimpour, A., Bakar, F. A., Mohamed, A. K. S., Forghani, B., Ab-Kadir, M. S. B., & Saari, N. (2012). A glutamic acid-producing lactic acid bacteria isolated from Malaysian fermented foods. International Journal of Molecular Sciences, 13(5), 5482-5497. https://doi.org/10.3390/ijms13055482

Zhang, Y., Zhu, M., Lu, W., Zhang, C., Chen, D., Shah, N. P., & Xiao, C. (2023). Optimizing Levilactobacillus brevis NPS-QW 145 fermentation for gamma-aminobutyric acid (GABA) production in soybean sprout yogurt-like product. Foods, 12(5), 977. https://doi.org/10.3390/foods12050977

Zheng, J., Wittouck, S., Salvetti, E., Franz, C., Harris, H., Mattarell, P., O’Toole, P., Pot, B., Vandamme, P., Walter, J., Watanabe, K., Wuyts, S., Felis, G., Gänzle, M., & Lebeer, S. (2020). A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. International Journal of Systematic and Evolutionary Microbiology, 70, 2782-2858. https://doi.org/10.1099/ijsem.0.004107

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