Metagenomic analysis of the bacterial community and gamma-aminobutyric acid (GABA) synthesis by lactic acid bacteria from seredele, a Balinese fermented soybean product
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Abstract. Kusumaningsih P, Jatmiko YD, Kusumawati IGA, Nursini NW, Yogeswara IBA. 2024. Metagenomic analysis of the bacterial community and gamma-aminobutyric acid (GABA) synthesis by lactic acid bacteria from seredele, a Balinese fermented soybean product. Biodiversitas 25: 4190-4198. Seredele is a fermented Balinese soybean product that undergoes spontaneous fermentation for two days at room temperature. This fermented food, commonly consumed as a condiment, has a distinctive smell similar to Japanese natto. The bacterial dynamics during fermentation using a metagenomic approach have not been reported. This study aimed to reveal bacterial dynamics during seredele fermentation and to obtain gamma-aminobutyric acid (GABA)-producing lactic acid bacteria from seredele. The bacterial dynamics of seredele were investigated using 16S rRNA sequencing. Lactic acid bacteria (LAB) were also isolated and screened for their ability to produce GABA. The metagenomics analysis showed that Weissella, Streptococcus, and Enterococcus are the most prevalent bacterial genera during fermentation. The relative abundance of bacteria at the species level indicates that W. confusa, W. paramesenteroides, E. faecium, S. lutetiensis, and E. durans are the most abundant bacteria at all stages of fermentation. Consistent with the metagenomic analysis, two strains, Limosilactobacillus fermentum A7304 and Enterococcus lactis A7303, produced 60 mg/L and 65 mg/L of GABA, respectively, in de Man Rogosa (MRS) medium enriched with 1% monosodium glutamate (MSG). This work opens opportunities to understand the bacterial dynamics in seredele and its potential as a source of GABA-producing bacteria.
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References
Abe Y, Umemura S, Sugimoto K, Hirawa N, Kato Y, Yokoyama N, Yokoyama T, Iwai J, Ishii M. 1995. Effect of green tea rich in??-aminobutyric acid on blood pressure of dahl salt-sensitive rats. Am J Hypertens 8 (1): 74-79. DOI: 10.1016/0895-7061(94)00141-w.
Afzaal M, Saeed F, Islam F, Ateeq H, Asghar A, Shah YA, Ofoedu CE, Chacha JS. 2022. Nutritional health perspective of natto: A critical review. Biochem Res Intl 2022: 5863887. DOI: 10.1155/2022/5863887.
Carafa I, Stocco G, Nardin T, Larcher R, Bittante G, Tuohy K, Franciosi E. 2019. Production of naturally ?-aminobutyric acid-enriched cheese using the dairy strains Streptococcus thermophilus 84C and Lactobacillus brevis DSM 32386. Front Microbiol 10: 93. DOI: 10.3389/fmicb.2019.00093.
Cho YR, Chang JY, Chang HC. 2007. Production of?gamma-aminobutyric acid (GABA) by Lactobacillus buchneri isolated from kimchi and its neuroprotective effect on neuronal cells. J Microbiol Biotechnol 17 (1): 104-109.
De Coster W, D’Hert S, Schultz DT, Cruts M, Broeckhoven CV. 2018. NanoPack: Visualizing and processing long-read sequencing data. Bioinformatics 34: 2666-2669. DOI: 10.1093/bioinformatics/bty149.
D’Este M, Alvarado-Morales M, IAngelidaki I. 2018. Amino acids production focusing on fermentation technologies - A review. Biotechnol Adv 36: 14-25. DOI: 10.1016/j.biotechadv.2017.09.001.
Diez-Gutiérrez L, Vicente LS, Barron LJR, Villaran MDC, Chavarri M. 2020. Gamma-aminobutyric acid and probiotics: Multiple health benefits and their future in the global functional food and nutraceuticals market. J Functional Foods 64: 103669. DOI: 10.1016/j.jff.2019.103669.
Fessard A, Remize F. 2017. Why are Weissella spp. not used as commercial starter cultures for food fermentation?. Fermentation 3 (3): 38. DOI: 10.3390/fermentation3030038.
Franciosi E, Carafa I, Nardin T, Schiavon S, Poznanski E, Cavazza A, Larcher R, Tuohy KM. 2015. Biodiversity and?? -aminobutyric acid production by lactic acid bacteria isolated from traditional alpine raw cow’s milk cheeses. BioMed Res Intl 2015: 625740. DOI: 10.1155/2015/625740.
Fusco V, Quero GM, Cho G-S, Kabisch, J, Meske D, Neve H, Bockelmann W, Franz CMAP. 2015. The genus Weissella: Taxonomy, ecology and biotechnological potential. Front Microbiol 6: 155. DOI: 10.3389/fmicb.2015.00155.
Hepsomali P, Groeger JA, Nishihira J, Scholey A. 2020. Effects of oral gamma-aminobutyric acid (GABA) administration on stress and sleep in humans: A systematic review. Front Neurosci 14: 923. DOI: 10.3389/fnins.2020.00923.
Hong K-B Park Y, Suh HJ. 2016. Sleep-promoting effects of the GABA/5-HTP mixture in vertebrate models. Behav Brain Res 310: 36-41. DOI: 10.1016/j.bbr.2016.04.049.
Jeong D-W, Kim H-R, Jung G, Han S, Kim C-T, Lee J-H. 2014. Bacterial community migration in the ripening of doenjang, a traditional Korean fermented soybean food. J Microbiol Biotechnol 24 (5): 648-660. DOI: 10.4014/jmb.1401.01009.
Joishy TK, Dehingia M, Khan MR. 2019. Bacterial diversity and metabolite profiles of curd prepared by natural fermentation of raw milk and back sloping of boiled milk. World J Microbiol Biotechnol 35 (7): 102. DOI: 10.1007/s11274-019-2677-y.
Jung WY, Jung JY, Lee HJ, Jeon CO. 2016. Functional characterization of bacterial communities responsible for fermentation of doenjang: A traditional korean fermented soybean paste. Front Microbiol 7: 827. DOI: 10.3389/fmicb.2016.00827.
Kaur S, Sharma P, Mayer MJ, Neuret S, Narbad A, Kaur S. 2023. Beneficial effects of GABA-producing potential probiotic Limosilactobacillus fermentum L18 of human origin on intestinal permeability and human gut microbiota. Microb Cell Fact 22: 256. DOI: 10.1186/s12934-023-02264-2.
Kharnaior P, Tamang JP. 2021. Bacterial and fungal communities and their predictive functional profiles in kinema, a naturally fermented soybean food of India, Nepal and Bhutan. Food Res Int 140: 110055. DOI: 10.1016/j.foodres.2020.110055.
Kharnaior P, Tamang JP. 2023. Probiotic properties of lactic acid bacteria isolated from the spontaneously fermented soybean foods of the eastern Himalayas. Fermentation 9: 461. DOI: 10.3390/fermentation9050461.
Kim D, Song L, Breitwieser FP, Salzberg SL. 2016. Centrifuge: Rapid and sensitive classification of metagenomic sequences. Genome Res 26 (12): 1721-1729. DOI: 10.1101/gr.210641.116.
Komatsuzaki N, Shima J, Kawamoto S, Momose H, Kimura T. 2005. Production of ?-aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiol 22 (6): 497-504. DOI: 10.1016/j.fm.2005.01.002.
Kwofie MK, Bukari N, Adeboye O. 2020. Probiotics potential of yeast and lactic acid bacteria fermented foods and the impact of processing: A review of indigenous and continental food products. Adv Microbiol 10 (9): 492-507. DOI: 10.4236/aim.2020.109037.
Lu X, Chen Z, Gu Z, Han Y. 2008. Isolation of? ? -aminobutyric acid-producing bacteria and optimization of fermentative medium. Biochem Eng J 41 (1): 48-52. DOI: 10.1016/j.bej.2008.03.005.
Lyu C-J, Liu L, Huang J, Zhao W-R, Hu S, Mei L-H, Yao S-J. 2019. Biosynthesis of ?-aminobutyrate by engineered Lactobacillus brevis cells immobilized in gellan gum gel beads. J Biosci Bioeng 128 (2): 123-128. DOI: 10.1016/j.jbiosc.2019.01.010.
Mandhania MH, Paul D, Suryavanshi MV, Sharma L, Chowdury S, Diwanay, SS, Diwanay SS, Shouche YS, Patole MS. 2019. Diversity and succession of microbiota during fermentation of the traditional Indian food idli. Appl Environ Microbiol 85 (13): e00368-19. DOI: 10.1128/AEM.00368-19.
Marco ML, Heeney D, Binda S, Cifelli CJ, Cotter PD, Foligné B, Gänzle M, Kort R, Pasin G, Pihlanto A, Smid EJ, Hutkins R. 2017. Health benefits of fermented foods: Microbiota and beyond. Curr Opin Biotechnol 44: 94-102. DOI: 10.1016/j.copbio.2016.11.010.
Nakamura H, Takishima T, Kometani T, Yokogoshi H. 2009. Psychological stress-reducing effect of chocolate enriched with ?-aminobutyric acid (GABA) in humans: Assessment of stress using heart rate variability and salivary chromogranin A. Intl J Food Sci Nutr 60: 106-113. DOI: 10.1080/09637480802558508.
Nam Y-D, Yi S-H, Lim S-I. 2012. Bacterial diversity of cheonggukjang, a traditional Korean fermented food, analyzed by barcoded pyrosequencing. Food Control 28: 135-142. DOI: 10.1016/j.foodcont.2012.04.028.
Nygaard AB, Tunsjø HS, Meisal R, Charnock C. 2020. A preliminary study on the potential of nanopore MinION and Illumina MiSeq 16S RRNA gene sequencing to characterize building-dust microbiomes. Sci Rep 10: 3209. DOI: 10.1038/s41598-020-59771-0.
Ratanaburee A, Kantachote D, Charernjiratrakul W, Sukhoom A. 2013. Selection of ?-aminobutyric acid-producing lactic acid bacteria and their potential as probiotics for use as starter cultures in Thai fermented sausages (Nham). Intl J Food Sci Technol 48 (7): 1371-1382. DOI: 10.1111/ijfs.12098.
Ribeiro SC, Domingos-Lopes MFP, Stanton C, Ross RP, Silva CCG. 2018. Production of ?-Aminobutyric Acid (GABA) by Lactobacillus otakiensis and other Lactobacillus sp. isolated from traditional Pico cheese. Intl J Dairy Technol 71 (4): 1012-1017. DOI: 10.1111/1471-0307.12527.
Sabna BS, Thankappan B, Mahendran R, Muthusamy G, Selta DJF, Angaryakanni J. 2021. Evaluation of GABA production and probiotic activities of Enterococcus faecium BS5. Probiotics Antimicrob Prot 13: 993-1004. DOI: 10.1007/s12602-021-09759-7.
Sanchart C, Rattanaporn O, Haltrich D, Phukpattaranont P, Maneerat S. 2017. Lactobacillus futsaii CS3, a new GABA-producing strain isolated from Thai fermented shrimp (kung-som). Indian J Microbiol 57 (2): 211-217. DOI: 10.1007/s12088-016-0632-2.
Seo YC, Choi WY, Kim JS, Lee CG, Ahn JH, Cho HY, Lee SH, Cho JS, Joo SJ, Lee HY. 2012. Enhancement of the cognitive effects of??-aminobutyric acid from monosodium glutamate fermentation by Lactobacillus sakei B2-16. Food Biotechnol 26 (1): 29-44. DOI: 10.1080/08905436.2011.645937.
Shi F, Li Y. 2011. Synthesis of ?-aminobutyric acid by expressing Lactobacillus brevis-derived glutamate decarboxylase in the Corynebacterium glutamicum strain ATCC 13032. Biotechnol Lett 33 (12): 2469-2474. DOI: 10.1007/s10529-011-0723-4.
Siragusa S, de Angelis M, di Cagno R, Rizzello CG, Coda R, Gobbetti M. 2007. Synthesis of?? aminobutyric acid by lactic acid bacteria isolated from a variety of Italian cheeses. Appl Environ Microbiol 73 (22): 7283-7290. DOI: 10.1128/AEM.01064-07.
Sumarmono J, Kusuma RJ, Rahayu N, Sukarno AS, Wulansari PD. 2023. Metagenomic analysis of the microbial community in kefir grains from different milk sources. Biodiversitas 24 (10): 5302-5308. DOI: 10.13057/biodiv/d241011.
Suparthana, IP, Duniaji AS, Hashimoto M. 2018. Investigation to traditionally produced soybean fermented food (sere kedele) in Gianyar Region-Bali and molecular identification of bacteria involved in their spontaneous fermentation. Sci J Food Technol 5 (2): 66-72.
Tang D, Chen M, Huang X, Zhang G, Zeng L. Zhang G, Wu S, Wang Y. 2023. SRplot: A free online platform for data visualization and graphing. PLoS One 18: e0294236. DOI: 10.1371/journal.pone.0294236.
Wick RR, Judd LM, Holt KE. 2019. Performance of neural network basecalling tools for Oxford nanopore sequencing. Genome Biol 20: 129. DOI: 10.1186/s13059-019-1727-y.
Wongsurawat T, Sutheeworapong S, Jenjaroenpun P, Charoensiddhi S, Khoiri AN, Topanurak S, Sutthikornchai C, Jintaridth P. 2023. Microbiome analysis of Thai traditional fermented soybeans reveals short-chain fatty acid-associated bacterial taxa. Sci Rep 13: 7573. DOI: 10.1038/s41598-023-34818-0.
Wu JR, Zhang JC, Shi P, Wu R, Yue XQ, Zhang HP. 2013. Bacterial community involved in traditional fermented soybean paste dajiang made in northeast China. Ann Microbiol 63: 1417-1421. DOI: 10.1007/s13213-013-0604-2.
Xie M, An F, Zhao Y, Wu R, Wu J. 2020. Metagenomic analysis of bacterial community structure and functions during the fermentation of da-jiang, a Chinese traditional fermented food. LWT 129: 109450. DOI: 10.1016/j.lwt.2020.109450.
Yogeswara IBA, Kusumawati IGAW, Sumadewi NLU, Rahayu ES, Indrati R. 2018. Isolation and identification of lactic acid bacteria from Indonesian fermented foods as ?-aminobutyric acid-producing bacteria. Intl Food Res J 25: 1753-1757. DOI: 10.5555/20193000525.
Yogeswara IBA, Kittibunchakul S, Rahayu ES, Domig KJ, Haltrich D, Nguyen TH. 2021. Microbial production and enzymatic biosynthesis of ?-aminobutyric acid (GABA) using Lactobacillus plantarum FNCC 260 isolated from Indonesian fermented foods. Processes 9 (1): 22. DOI: 10.3390/pr9010022.
Yongsawas R, In-on A, Inta A, Kampuansai J, Pandith H, Suwannarach N, Lumyong S, Chitov T, Disayathanoowat T. 2023. Bacterial communities in lanna fermented soybeans from three different ethnolinguistic groups in northern Thailand, Microorganisms 11 (3): 649. DOI: 10.3390/microorganisms11030649.