Hybrid substrate-based pH autobuffering GABA fermentation by Levilactobacillus brevis CD0817.

Levilactobacillus brevis CD0817 Gamma-aminobutyric acid Monosodium L-glutamate Powdery L-glutamic acid pH autobuffering fermentation

Journal

Bioprocess and biosystems engineering
ISSN: 1615-7605
Titre abrégé: Bioprocess Biosyst Eng
Pays: Germany
ID NLM: 101088505

Informations de publication

Date de publication:
13 Sep 2024
Historique:
received: 30 05 2024
accepted: 07 09 2024
medline: 13 9 2024
pubmed: 13 9 2024
entrez: 13 9 2024
Statut: aheadofprint

Résumé

The probiotic fermentation of the bioactive substance gamma-aminobutyric acid (GABA) is an attractive research topic. There is still room for further improvement in reported GABA fermentation methods based on a single substrate (L-glutamic acid or L-monosodium glutamate). Here, we devised a pH auto-buffering strategy to facilitate the fermentation of GABA by Levilactobacillus brevis CD0817. This strategy features a mixture of neutral monosodium L-glutamate plus acidic L-glutamic acid as the substrate. This mixture provides a mild initial pH; moreover, the newly dissolved L-glutamic acid automatically offsets the pH increase caused by substrate decarboxylation, maintaining the acidity essential for GABA fermentation. In this study, a flask trial was first performed to optimize the GABA fermentation parameters of Levilactobacillus brevis CD0817. The optimized parameters were further validated in a 10 L fermenter. The flask trial results revealed that the appropriate fermentation medium was composed of powdery L-glutamic acid (750 g/L), monosodium L-glutamate (34 g/L [0.2 mol/L]), glucose (5 g/L), yeast extract (35 g/L), MnSO

Identifiants

pubmed: 39269502
doi: 10.1007/s00449-024-03088-z
pii: 10.1007/s00449-024-03088-z
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Innovative Research Group Project of the National Natural Science Foundation of China
ID : 32160014
Organisme : the Major Discipline Academic and Technical Leaders Training Program of Jiangxi Province
ID : 20225BCJ22023

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Duranti S, Ruiz L, Lugli GA et al (2020) Bifidobacterium adolescentis as a key member of the human gut microbiota in the production of GABA. Sci Rep 10:14112. https://doi.org/10.1038/s41598-020-70986-z
doi: 10.1038/s41598-020-70986-z pubmed: 32839473 pmcid: 7445748
Sarasa SB, Mahendran R, Muthusamy G et al (2020) A brief review on the non-protein amino acid, gamma-amino butyric acid (GABA): its production and role in microbes. Curr Microbiol 77:534–544. https://doi.org/10.1007/s00284-019-01839-w
doi: 10.1007/s00284-019-01839-w pubmed: 31844936
Liu F, Zhang H, Zhang X et al (2023) Site-directed mutagenesis improves the practical application of L-glutamic acid decarboxylase in Escherichia coli. Eng Life Sci 23:e2200064. https://doi.org/10.1002/elsc.202200064
doi: 10.1002/elsc.202200064
He W, Song H, Yang Z et al (2023) Beneficial effect of GABA-rich fermented milk whey on nervous system and intestinal microenvironment of aging mice induced by D-galactose. Microbiol Res 278:127547. https://doi.org/10.1016/j.micres.2023.127547
doi: 10.1016/j.micres.2023.127547 pubmed: 37976737
Sun Y, Mehmood A, Giampieri F et al (2023) Insights into the cellular, molecular, and epigenetic targets of gamma-aminobutyric acid against diabetes: a comprehensive review on its mechanisms. Crit Rev Food Sci Nutr. https://doi.org/10.1080/10408398.2023.2255666
doi: 10.1080/10408398.2023.2255666 pubmed: 38149655
Shi Y (2022) Linking B cell metabolism to immune regulation: the neurotransmitter GABA. Signal Transduct Target Ther 7:260. https://doi.org/10.1038/s41392-022-01120-w
doi: 10.1038/s41392-022-01120-w pubmed: 35915062 pmcid: 9340731
Liu W, Li H, Liu L et al (2023) γ-aminobutyric acid produced by Levilactobacillus brevis using Chinese cabbage waste. Food Sci Technol. https://doi.org/10.1016/j.lwt.2023.114691
doi: 10.1016/j.lwt.2023.114691
Binh TT, Ju WT, Jung WJ et al (2014) Optimization of gamma-amino butyric acid production in a newly isolated Lactobacillus brevis. Biotechnol Lett 36:93–98. https://doi.org/10.1007/s10529-013-1326-z
doi: 10.1007/s10529-013-1326-z pubmed: 24078124
Liu WL, Li HM, Liu L et al (2022) Screening of gamma-aminobutyric acid-producing lactic acid bacteria and the characteristic of glutamate decarboxylase from Levilactobacillus brevis F109-MD3 isolated from kimchi. J Appl Microbiol 132:1967–1977. https://doi.org/10.1111/jam.15306
doi: 10.1111/jam.15306 pubmed: 34570423
Huang J, Mei L, Sheng Q et al (2007) Purification and characterization of glutamate decarboxylase of Lactobacillus brevis CGMCC 1306 isolated from fresh milk. Chin J Chem Eng 15:157–161. https://doi.org/10.1016/s1004-9541(07)60051-2
doi: 10.1016/s1004-9541(07)60051-2
Wu Q, Shah NP (2017) High gamma-aminobutyric acid production from lactic acid bacteria: emphasis on Lactobacillus brevis as a functional dairy starter. Crit Rev Food Sci Nutr 57:3661–3672. https://doi.org/10.1080/10408398.2016.1147418
doi: 10.1080/10408398.2016.1147418 pubmed: 26980301
Mousavi R, Mottawea W, Hassan H et al (2022) Screening, characterization and growth of gamma-aminobutyric acid-producing probiotic candidates from food origin under simulated colonic conditions. J Appl Microbiol 132:4452–4465. https://doi.org/10.1111/jam.15550
doi: 10.1111/jam.15550 pubmed: 35338685
Ham S, Bhatia SK, Gurav R et al (2022) Gamma aminobutyric acid (GABA) production in Escherichia coli with pyridoxal kinase (pdxY) based regeneration system. Enzyme Microb Technol 155:109994. https://doi.org/10.1016/j.enzmictec.2022.109994
doi: 10.1016/j.enzmictec.2022.109994 pubmed: 35077875
Lee SJ, Jeon HS, Yoo JY et al (2022) Characterization of a novel glutamate decarboxylase (GAD) from Latilactobacillus curvatus K285 isolated from Gat -Kimchi. Food Sci Biotechnol 31:69–78. https://doi.org/10.1007/s10068-021-01005-8
doi: 10.1007/s10068-021-01005-8 pubmed: 35059231
Fan X, Yu L, Shi Z et al (2023) Characterization of a novel flavored yogurt enriched in gamma-aminobutyric acid fermented by Levilactobacillus brevis CGMCC1.5954. J Dairy Sci 106:852–867. https://doi.org/10.3168/jds.2022-22590
doi: 10.3168/jds.2022-22590 pubmed: 36494222
Liu H, Liu D, Zhang C et al (2024) Whole-genome analysis, evaluation and regulation of in vitro and in vivo GABA production from Levilactobacillus brevis YSJ3. Int J Food Microbiol 421:110787. https://doi.org/10.1016/j.ijfoodmicro.2024.110787
doi: 10.1016/j.ijfoodmicro.2024.110787 pubmed: 38878704
Xie X, Ro KS, Wu H et al (2023) A novel γ-aminobutyric acid biosynthetic pathway in Lentilactobacillus curieae CCTCC M 2011381T. Process Biochem 124:160–167. https://doi.org/10.1016/j.procbio.2022.11.013
doi: 10.1016/j.procbio.2022.11.013
Villegas JM, Brown L, Savoy de Giori G et al (2016) Optimization of batch culture conditions for GABA production by Lactobacillus brevis CRL 1942, isolated from quinoa sourdough. LWT-Food Sci Technol 67:22–26. https://doi.org/10.1016/j.lwt.2015.11.027
doi: 10.1016/j.lwt.2015.11.027
Kotik M (2009) Novel genes retrieved from environmental DNA by polymerase chain reaction: current genome-walking techniques for future metagenome applications. J Biotechnol 144:75–82. https://doi.org/10.1016/j.jbiotec.2009.08.013
doi: 10.1016/j.jbiotec.2009.08.013 pubmed: 19712711
Wang L, Jia M, Li Z et al (2022) Wristwatch PCR: a versatile and efficient genome walking strategy. Front Bioeng Biotechnol 10:792848. https://doi.org/10.3389/fbioe.2022.792848
doi: 10.3389/fbioe.2022.792848 pubmed: 35497369 pmcid: 9039356
Wang L, Jia M, Li Z et al (2023) Protocol to access unknown flanking DNA sequences using Wristwatch-PCR for genome-walking. STAR Protoc 4:102037. https://doi.org/10.1016/j.xpro.2022.102037
doi: 10.1016/j.xpro.2022.102037 pubmed: 36853735 pmcid: 9871321
Luo H, Liu Z, Xie F et al (2021) Microbial production of gamma-aminobutyric acid: applications, state-of-the-art achievements, and future perspectives. Crit Rev Biotechnol 41:491–512. https://doi.org/10.1080/07388551.2020.1869688
doi: 10.1080/07388551.2020.1869688 pubmed: 33541153
Park SJ, Kim DH, Kang HJ et al (2021) Enhanced production of γ-aminobutyric acid (GABA) using Lactobacillus plantarum EJ2014 with simple medium composition. Food Sci Technol 137:110443. https://doi.org/10.1016/j.lwt.2020.110443
doi: 10.1016/j.lwt.2020.110443
Shi X, Chang C, Ma S et al (2017) Efficient bioconversion of L-glutamate to gamma-aminobutyric acid by Lactobacillus brevis resting cells. J Ind Microbiol Biotechnol 44:697–704. https://doi.org/10.1007/s10295-016-1777-z
doi: 10.1007/s10295-016-1777-z pubmed: 27155855
Wang Q, Liu X, Fu J et al (2018) Substrate sustained release-based high efficacy biosynthesis of GABA by Lactobacillus brevis NCL912. Microb Cell Fact 17:80. https://doi.org/10.1186/s12934-018-0919-6
doi: 10.1186/s12934-018-0919-6 pubmed: 29778094 pmcid: 5960080
Choi JW, Yim SS, Lee SH et al (2015) Enhanced production of gamma-aminobutyrate (GABA) in recombinant Corynebacterium glutamicum by expressing glutamate decarboxylase active in expanded pH range. Microb Cell Fact 14:21. https://doi.org/10.1186/s12934-015-0205-9
doi: 10.1186/s12934-015-0205-9 pubmed: 25886194 pmcid: 4335662
Li H, Qiu T, Chen Y et al (2011) Separation of gamma-aminobutyric acid from fermented broth. J Ind Microbiol Biotechnol 38:1955–1959. https://doi.org/10.1007/s10295-011-0984-x
doi: 10.1007/s10295-011-0984-x pubmed: 21614609
Pannerchelvan S, Rios-Solis L, Wong FWF et al (2023) Strategies for improvement of gamma-aminobutyric acid (GABA) biosynthesis via lactic acid bacteria (LAB) fermentation. Food Funct 14:3929–3948. https://doi.org/10.1039/d2fo03936b
doi: 10.1039/d2fo03936b pubmed: 36951915
Tames H, Sabater C, Margolles A et al (2023) Production of GABA in milk fermented by Bifidobacterium adolescentis strains selected on the bases of their technological and gastrointestinal performance. Food Res Int 171:113009. https://doi.org/10.1016/j.foodres.2023.113009
doi: 10.1016/j.foodres.2023.113009 pubmed: 37330847
Chang F, Wang Y, Zhang J et al (2024) Efficient production of gamma-aminobutyric acid using engineered Escherichia coli whole-cell catalyst. Enzyme Microb Technol 174:110379. https://doi.org/10.1016/j.enzmictec.2023.110379
doi: 10.1016/j.enzmictec.2023.110379 pubmed: 38103484
Jia M, Zhu Y, Wang L et al (2022) pH auto-sustain-based fermentation supports efficient gamma-aminobutyric acid production by Lactobacillus brevis CD0817. Fermentation 8:208. https://doi.org/10.3390/fermentation8050208
doi: 10.3390/fermentation8050208
Li H, Sun T, Jia M et al (2022) Production of gamma-aminobutyric acid by Levilactobacillus brevis CD0817 by coupling fermentation with self-buffered whole-cell catalysis. Fermentation 8:321. https://doi.org/10.3390/fermentation8070321
doi: 10.3390/fermentation8070321
Gao D, Chang K, Ding G et al (2019) Genomic insights into a robust gamma-aminobutyric acid-producer Lactobacillus brevis CD0817. AMB Express 9:72. https://doi.org/10.1186/s13568-019-0799-0
doi: 10.1186/s13568-019-0799-0 pubmed: 31127390 pmcid: 6534642
Li H, Pei J, Wei C et al (2023) Sodium-Ion-Free Fermentative Production of GABA with Levilactobacillus brevis CD0817. Metabolites. https://doi.org/10.3390/metabo13050608
doi: 10.3390/metabo13050608 pubmed: 38248820 pmcid: 10818445
Li H, Wang L, Nie L et al (2023) Sensitivity intensified ninhydrin-based chromogenic system by ethanol-ethyl acetate: application to relative quantitation of GABA. Metabolites 13:283. https://doi.org/10.3390/metabo13020283
doi: 10.3390/metabo13020283 pubmed: 36837902 pmcid: 9966720
Chen Y, Chang K, Xie X et al (2019) Disassociation of glutamate from gamma-aminobutyric acid by zinc acetate-assisted differential precipitation/dissolution: application to the quantification of gamma-aminobutyric acid. J Chromatogr A 1590:19–26. https://doi.org/10.1016/j.chroma.2019.01.002
doi: 10.1016/j.chroma.2019.01.002 pubmed: 30638713
Cui Y, Miao K, Niyaphorn S et al (2020) Production of gamma-aminobutyric acid from lactic acid bacteria: a systematic review. Int J Mol Sci 21:995. https://doi.org/10.3390/ijms21030995
doi: 10.3390/ijms21030995 pubmed: 32028587 pmcid: 7037312
Cha X, Ding J, Ba W et al (2023) High production of gamma-aminobutyric acid by activating the xyl operon of Lactobacillus brevis. ACS Omega 8:8101–8109. https://doi.org/10.1021/acsomega.2c08272
doi: 10.1021/acsomega.2c08272 pubmed: 36873027 pmcid: 9979331
Galli V, Venturi M, Mari E et al (2022) Gamma-aminobutyric acid (GABA) production in fermented milk by lactic acid bacteria isolated from spontaneous raw milk fermentation. Int Dairy J 127:105284. https://doi.org/10.1016/j.idairyj.2021.105284
doi: 10.1016/j.idairyj.2021.105284
Kim J, Yoon YW, Kim MS et al (2022) Gamma-aminobutyric acid fermentation in MRS-based medium by the fructophilic Lactiplantibacillus plantarum Y7. Food Sci Biotechnol 31:333–341. https://doi.org/10.1007/s10068-022-01035-w
doi: 10.1007/s10068-022-01035-w pubmed: 35273823 pmcid: 8885955
Zou XZ, Gong LC, Li TT et al (2024) Optimization of fermentation conditions for the production of gamma-aminobutyric acid by Lactobacillus hilgardii GZ2 from traditional Chinese fermented beverage system. Bioprocess Biosyst Eng 47:957–969. https://doi.org/10.1007/s00449-024-03028-x
doi: 10.1007/s00449-024-03028-x pubmed: 38717593
Falah F, Vasiee A, Tabatabaei-Yazdi F et al (2024) Optimization of γ-aminobutyric acid (GABA) production by Lactobacillus spp. from agro-food waste. Biomass Convers Biorefin 14:3425–3437. https://doi.org/10.1007/s13399-022-02361-z
doi: 10.1007/s13399-022-02361-z
Ding J, Ba W, You S et al (2023) Development of an oil-sealed anaerobic fermentation process for high production of γ-aminobutyric acid with Lactobacillus brevis isolated by directional colorimetric screening. Biochem Eng J. https://doi.org/10.1016/j.bej.2023.108893
doi: 10.1016/j.bej.2023.108893
Li H, Li B, Gao L et al (2023) Gamma-aminobutyric acid (GABA) promotes characteristics of Levilactobacillus sp. LB-2. LWT-Food Sci Technol 184:115014. https://doi.org/10.1016/j.lwt.2023.115014
doi: 10.1016/j.lwt.2023.115014
Kook MC, Seo MJ, Cheigh CI et al (2010) Enhanced production of gamma-aminobutyric acid using rice bran extracts by Lactobacillus sakei B2–16. J Microbiol Biotechnol 20:763–766. https://doi.org/10.4014/jmb.0911.11016
doi: 10.4014/jmb.0911.11016 pubmed: 20467250
Thongruck K, Maneerat S (2023) Enhanced production of gamma-aminobutyric acid (GABA) from Lactobacillus futsaii CS3 using agri-food industries by-products under batch and fed-batch fermentation. Indian J Microbiol 63:467-482. https://doi.org/10.1007/s12088-023-01101-9
doi: 10.1007/s12088-023-01101-9 pubmed: 38031599
Xiao T, Shah NP (2021) Lactic acid produced by Streptococcus thermophilus activated glutamate decarboxylase (GadA) in Lactobacillus brevis NPS-QW 145 to improve γ-amino butyric acid production during soymilk fermentation. LWT-Food Sci Technol 137:110474. https://doi.org/10.1016/j.lwt.2020.110474
doi: 10.1016/j.lwt.2020.110474
Zhang Y, Zhu M, Lu W et al (2023) Optimizing Levilactobacillus brevis NPS-QW 145 fermentation for gamma-aminobutyric acid (GABA) production in soybean sprout yogurt-like product. Foods. https://doi.org/10.3390/foods12050977
Guo T, Zhang L, Xin Y et al (2017) Oxygen-inducible conversion of lactate to acetate in heterofermentative Lactobacillus brevis ATCC 367. Appl Environ Microbiol 83:e01659-e11617. https://doi.org/10.1128/AEM.01659-17
doi: 10.1128/AEM.01659-17 pubmed: 28842545 pmcid: 5648907
Lyu C, Zhao W, Peng C et al (2018) Exploring the contributions of two glutamate decarboxylase isozymes in Lactobacillus brevis to acid resistance and gamma-aminobutyric acid production. Microb Cell Fact 17:180. https://doi.org/10.1186/s12934-018-1029-1
doi: 10.1186/s12934-018-1029-1 pubmed: 30454056 pmcid: 6240960
Kim J, Lee MH, Kim MS et al (2022) Probiotic properties and optimization of gamma-aminobutyric acid production by Lactiplantibacillus plantarum FBT215. J Microbiol Biotechnol 32:783–791. https://doi.org/10.4014/jmb.2204.04029
doi: 10.4014/jmb.2204.04029 pubmed: 35586927 pmcid: 9628908
Tanamool V, Hongsachart P, Soemphol W (2020) 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
doi: 10.1590/fst.05419
Abbasiliasi S, Tan JS, Tengku Ibrahim TA et al (2017) Fermentation factors influencing the production of bacteriocins by lactic acid bacteria: a review. RSC Adv 7:29395–29420. https://doi.org/10.1039/c6ra24579j
doi: 10.1039/c6ra24579j
Thu Ho NA, Hou CY, Kim WH et al (2013) Expanding the active pH range of Escherichia coli glutamate decarboxylase by breaking the cooperativeness. J Biosci Bioeng 115:154–158. https://doi.org/10.1016/j.jbiosc.2012.09.002
doi: 10.1016/j.jbiosc.2012.09.002 pubmed: 23026450
Huang J, Mei L, Wu H et al (2006) Biosynthesis of γ-aminobutyric acid (GABA) using immobilized whole cells of Lactobacillus brevis. World J Microbiol Biotechnol 23:865–871. https://doi.org/10.1007/s11274-006-9311-5
doi: 10.1007/s11274-006-9311-5
Wu CH, Hsueh YH, Kuo JM et al (2018) Characterization of a potential probiotic lactobacillus brevis RK03 and efficient production of γ-aminobutyric acid in batch fermentation. Int J Mol Sci 19:143. https://doi.org/10.3390/ijms19010143
doi: 10.3390/ijms19010143 pubmed: 29300336 pmcid: 5796092
Zhang L, Yue Y, Wang X et al (2022) Optimization of fermentation for gamma-aminobutyric acid (GABA) production by yeast Kluyveromyces marxianus C21 in okara (soybean residue). Bioprocess Biosyst Eng 45:1111–1123. https://doi.org/10.1007/s00449-022-02702-2
doi: 10.1007/s00449-022-02702-2 pubmed: 35179639
Asun AC, Lin ST, Ng HS et al (2022) Production of gamma-aminobutyric acid (GABA) by Bacillus subtilis BBEL02 fermentation using nitrogen-rich industrial wastes as crude feedstocks. Biochem Eng J 187:108654. https://doi.org/10.1016/j.bej.2022.108654
doi: 10.1016/j.bej.2022.108654

Auteurs

Lingqin Wang (L)

State Key Laboratory of Food Science and Resource, Nanchang University, Nanchang, 330047, China.
International Institute of Food Innovation Co., Ltd., Nanchang University, Nanchang, 330020, China.
Sino-German Joint Research Institute, Nanchang University, Nanchang, 330047, China.

Mengya Jia (M)

State Key Laboratory of Food Science and Resource, Nanchang University, Nanchang, 330047, China.
International Institute of Food Innovation Co., Ltd., Nanchang University, Nanchang, 330020, China.
Sino-German Joint Research Institute, Nanchang University, Nanchang, 330047, China.

Dandan Gao (D)

Biomedical Research Center, College of Life Sciences and Engineering, Northwest Minzu University, Lanzhou, 730030, China. gaodan0322@163.com.

Haixing Li (H)

State Key Laboratory of Food Science and Resource, Nanchang University, Nanchang, 330047, China. hxli@ncu.edu.cn.
International Institute of Food Innovation Co., Ltd., Nanchang University, Nanchang, 330020, China. hxli@ncu.edu.cn.
Sino-German Joint Research Institute, Nanchang University, Nanchang, 330047, China. hxli@ncu.edu.cn.

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