Gamma-Aminobutyric Acid (GABA) Producing Lactobacillus plantarum TSUB-17 and Probiotic Properties for Using as Probiotics Additive in Swine Feed
DOI:
https://doi.org/10.48048/tis.2024.7198Keywords:
Lactobacillus, GABA production, Probiotics properties, Swine feces, AntioxidantAbstract
Due to the use of probiotics in animal husbandry has recently increased, the selection of high-quality probiotic strains is crucial. Since the uses of probiotics for animal feed supplements have to be applied at high doses of bacteria to be effective, the cultures’ safety is essential. This study successfully isolated the novel Lactobacillus sp. from swine fecal samples and identified it as L. plantarum TSUB-17. The L. plantarum TSUB-17 exhibited excellent probiotic properties, including 100 % resistance to 3 % acids and 1 % bile salts, and effectively inhibits pathogenic bacteria such as Escherichia coli, Staphylococcus aureus, Pseudomonas aeruginosa, Klebsiella pneumoniae and Salmonella Typhimurium (isolated ESBL strain). L. plantarum TSUB-17 was also found to adhere to the intestinal wall and form a biofilm. Furthermore, the bacteria have revealed some unique properties of GABA production and detected the glutamate decarboxylase B (gadB) gene similar to L. brevis both in nucleotide sequence and secondary structure of the glutamate decarboxylase enzyme that was deduced from the nucleotide. The isolated bacteria also have antioxidant activity, and most importantly, the isolated strain was safe; it is non-hemolysis and susceptible to the tested antimicrobials. Therefore, L. plantarum TSUB-17 is suitable for further development as a probiotic additive in animal feed.
HIGHLIGHTS
- This study successfully isolated Lactobacillus plantarum TSUB-17 with a high potential to develop as a probiotic for animals. The isolated bacterium has excellent properties: It tolerates high levels of acids and bile salts. It is effective against many pathogenic bacteria, produces gamma-aminobutyric acid (GABA) and shows high levels of antioxidant activity. Moreover, L. plantarum TSUB-17 is very safe due to its non-hemolytic strain and susceptibility to numerous antimicrobial drugs.
GRAPHICAL ABSTRACT
Downloads
Metrics
References
M Even, S Davail, M Rey, A Tavernier, M Houssier, MD Bernadet, K Gontier, G Pascal and K Ricaud. Probiotics strains modulate gut microbiota and lipid metabolism in mule ducks. Open Microbiol. J. 2018; 12, 71-93.
BK Bajaj, IJJ Clae and S Lebeer. Functional mechanisms of probiotics. J. Microbiol. Biotechnol. Food Sci. 2015; 4, 321-7.
TG Smart and FA tephenson. A half century of γ-aminobutyric acid. Brain Neurosci. Adv. 2019; 3, 1-9.
I Hwang, K Jo, KC Shin, JI Kim, Y Ji, YJ Park, J Park, YG Jeon, S Ka, S Suk, HL Noh, SS Choe, AA Alfadda, JK Kim, S Kim and JB Kim. GABA-stimulated adipose-derived stem cells suppress subcutaneous adipose inflammation in obesity. Proc. Natl. Acad. Sci. 2019; 116, 11936-45.
Y Li, F Li, M Liu, J Yin, B Cheng, BM Shi and A Shan. Effect of γ-aminobutyric acid on growth performance, behavior and plasma hormones in weaned pigs. Can. J. Anim. Sci. 2015; 95, 165-71.
M Zhang, XT Zou, H Li, XY Dong and W Zhao. Effect of dietary γ-aminobutyric acid on laying performance, egg quality, immune activity and endocrine hormone in heat-stressed Roman hens. Anim. Sci. J. 2012; 83, 141-7.
XZ Xie, C Liang, MH Li and Z Chen. Effects of GABA on the thymus cytokines of Wenchang chickens submitted to heat stress. Braz. J. Poultry Sci. 2017; 17, 559-66.
NRM Sahab, E Subroto, RL Balia and GL Utama. γ-Aminobutyric acid found in fermented foods and beverages: Current trends. Heliyon 2020; 6, e05526.
D Rashmi, R Zanan, S John, K Khandagale and A Nadaf. Chapter 13 - γ-aminobutyric acid (GABA): Biosynthesis, role, commercial production, and applications, in studies in natural products. Stud. Nat. Prod. Chem. 2018; 57, 413-52.
Y Cui, K Miao, S Niyaphorn and X Qu. Production of gamma-aminobutyric acid from lactic acid bacteria: A systematic review. Int. J. Mol. Sci. 2020; 21, 995.
F Zarei, N Leila, EM Reza and MET Abadi. Production of amma-aminobutyric acid (GABA) in whey protein drink during fermentation by Lactobacillus plantarum. J. Microbiol. Biotechnol. Food Sci. 2021; 9, 1087-92.
H Li, T Qiu, G Huang and Y Cao. Production of gamma-aminobutyric acid by Lactobacillus brevis NCL912 using fed-batch fermentation. Microb. Cell Factories 2010; 9, 85.
R Dhakal, VK Bajpai and KH Baek. Production of GABA (γ-aminobutyric acid) by microorganisms: A review. Braz. J. Microbiol. 2012; 43, 1230-41.
N Amin, A Hussain, S Alamzeb and S Begum. Accumulation of heavy metals in edible parts of vegetables irrigated with waste water and their daily intake to adults and children, District Mardan, Pakistan. Food Chem. 2013; 136, 1515-23.
H Li, W Li, X Liu and Y Cao. gadA gene locus in Lactobacillus brevis NCL912 and its expression during fed-batch fermentation. FEMS Microbiol. Lett. 2013; 349, 108-16.
Q Wu, HM Tun, YS Law, E Khafipour and NP Shah. Common distribution of gad operon in Lactobacillus brevis and its GadA contributes to efficient GABA synthesis toward cytosolic near-neutral pH. Front. Microbiol. 2017; 8, 206.
E Karimian, A Moayedi, M Khomeiri, M Aalami and AS Mahoonak. Application of high-GABA producing Lactobacillus plantarum isolated from traditional cabbage pickle in the production of functional fermented whey-based formulate. J. Food Meas. Character 2020; 14, 3408-16.
N Komatsuzaki, J Shima, S Kawamoto, H Momose and T Kimura. Production of -aminobutyric acid (GABA) by Lactobacillus paracasei isolated from traditional fermented foods. Food Microbiol. 2005; 22, 497-504.
YR Cho, JY Chang and HC Chang. Production of gamma-aminobutyric acid (GABA) by Lactobacillus buchneri isolated from kimchi and its neuroprotective effect on neuronal cells. J. Microbiol. Biotechnol. 2007; 17, 104-9.
SS Bajic, J Djokic, M Dinic, K Veljovic, N Golic, S Mihajlovic and M Tolinacki. GABA-producing natural dairy isolate from artisanal Zlatar cheese attenuates gut inflammation and strengthens gut epithelial barrier in vitro. Front. Microbiol. 2019; 10, 527.
NB Silva, DA Longhi, WF Martins, JB Laurindo, GMF Aragão and BAM Carciofi. Modeling the growth of Lactobacillus viridescens under non-isothermal conditions in vacuum-packed sliced ham. Int. J. Food Microbiol. 2017; 240, 97-101.
E Patterson, PM Ryan, N Wiley, I Carafa, E Sherwin, G Moloney, E Franciosi, R Mandal, DS Wishart, K Tuohy, RP Ross, JF Cryan, TG Dinan and C Stanton. Gamma-aminobutyric acid-producing lactobacilli positively affect metabolism and depressive-like behaviour in a mouse model of metabolic syndrome. Sci. Rep. 2019; 9, 16323.
YL Chen, CC Lee, YL Lin, KM Yin, CL Ho and T Liu. Obtaining long 16S rDNA sequences using multiple primers and its application on dioxin-containing samples. BMC Bioinformatics 2015; 16, S13.
B Arabpour, A Esmaeili and M Rabbani. Cloning and expression vector construction of glutamate decarboxylase gene from Lactobacillus plantarum. J. Babol Univ. Med. Sci. 2016; 18, 66-72.
H Thomas. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. 1991; 41, 95-8.
A Waterhouse, M Bertoni, S Bienert, G Studer, G Tauriello, R Gumienny, FT Heer, TAP de Beer, C Rempfer, L Bordoli, R Lepore and T Schwede. Swiss-model: Homology modelling of protein structures and complexes. Nucleic Acids Res. 2018; 46, W296-303.
S Baliyan, R Mukherjee, A Priyadarshini, A Vibhuti, A Gupta, RP Pandey and CM Chang. Determination of antioxidants by DPPH radical scavenging activity and quantitative phytochemical analysis of Ficus religiosa. Molecules 2022; 27, 1326.
M Lertworapreecha, S Noomee, S Sutthimusik, B Utarapicha and K Tontikapong. Multidrug resistant and extended spectrum b-lactamase producing Salmonella enterica isolated from food animals in Phatthalung, Thailand. Southeast Asian J. Trop. Med. Publ. Health 2016; 47, 1257-69.
L Jin, Y Ho, N Abdullah and S Jalaludin. Acid and bile tolerance of Lactobacillus isolated from chicken intestine. Lett. Appl. Microbiol. 1998; 27, 183-5.
P Thomas, A C Sekhar, R Upreti, MM Mujawar and SS Pasha. Optimization of single plate-serial dilution spotting (SP-SDS) with sample anchoring as an assured method for bacterial and yeast cfu enumeration and single colony isolation from diverse samples. Biotechnol. Rep. 2015; 8, 45-55.
J Huang, W Zhang, Z Hu, Z Liu, T Du, Y Dai and T Xiong. Isolation, characterization and selection of potential probiotic lactic acid bacteria from feces of wild boar, native pig and commercial pig. Livest. Sci. 2020; 237, 104036.
EM Tuomola and SJ Salminen. Adhesion of some probiotic and dairy Lactobacillus strains to Caco-2 cell cultures. Int. J. Food. Microbiol. 1998; 41, 45-51.
GA O’Toole. Microtiter dish biofilm formation assay. J. Vis. Exp. 2011; 47, 2437.
Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing M100-S27. Clinical and Laboratory Standards Institute, Wayne, Pennsylvania, 2017.
F Cobo, V Pérez-Carrasco, L Martín-Hita, JA García-Salcedo and JM Navarro-Marí. Comparative evaluation of MALDI-TOF MS and 16S rRNA gene sequencing for the identification of clinically relevant anaerobic bacteria. Critical evaluation of discrepant results. Anaerobe 2023; 82, 102754.
P Markowiak and K Śliżewska. The role of probiotics, prebiotics and synbiotics in animal nutrition. Gut Pathogens 2018; 10, 21.
Food and Agriculture Organization and World Health Organization. Guidelines for the evaluation of probiotics in food. Food and Agriculture Organization and World Health Organization, London Ontario, Canada, 2002.
I Stefańska, E Kwiecień, K Jóźwiak-Piasecka, M Garbowska, M Binek and M Rzewuska. Antimicrobial susceptibility of lactic acid bacteria strains of potential use as feed additives - the basic safety and usefulness criterion. Front. Vet. Sci. 2021; 8, 687071.
M Dec, R Urban-Chmiel, D Stępień-Pyśniak and A Wernicki. Assessment of antibiotic susceptibility in Lactobacillus isolates from chickens. Gut Pathogens 2017; 9, 54.
I Campedelli, H Mathur, E Salvetti, S Clarke, MC Rea, S Torriani, RP Ross, C Hill and PW O’Toole. Genus-wide assessment of antibiotic resistance in Lactobacillus spp. Appl. Environ. Microbiol. 2019; 85, e01738-18.
YM Álvarez-Cisneros and E Ponce-Alquicira. Antibiotic resistance in lactic acid bacteria. In: Y Kumar (Ed.). Antimicrobial resistance: A global threat. Intech Open, Rijeka, Croatia, 2018.
EJC Goldstein, KL Tyrrell and DM Citron. Lactobacillus species: Taxonomic complexity and controversial susceptibilities. Clin. Infect. Dis. 2015, 60, S98-107.
P Sharma, SK Tomar, V Sangwan, P Goswami and R Singh. Antibiotic resistance of Lactobacillus sp. isolated from commercial probiotic preparations. J. Food Saf. 2016, 36, 38-51.
E Anisimova, I Gorokhova, G Karimullina and D Yarullina. Alarming antibiotic resistance of Lactobacilli isolated from probiotic preparations and dietary supplements. Antibiotics 2022; 11, 1557.
BA Behbahani, H Jooyandeh, F Falah and A Vasiee. Gamma-aminobutyric acid production by Lactobacillus brevis A3: Optimization of production, antioxidant potential, cell toxicity, and antimicrobial activity. Food Sci. Nutr. 2020; 8, 5330-9.
X Cha, J Ding, W Ba, S You, W Qi and R Su. High production of γ-aminobutyric acid by activating the xyl operon of Lactobacillus brevis. ACS Omega 2023; 8, 8101-9.
RA Yunes, EU Poluektova, MS Dyachkova, KM Klimina, AS Kovtun, OV Averina, VS Orlova and VN Danilenko. GABA production and structure of gadB/gadC genes in Lactobacillus and Bifidobacterium strains from human microbiota. Anaerobe 2016; 42, 197-204.
A Yasiri and S Seubsasana. Isolation of bile salt hydrolase and uricase producing Lactobacillus brevis SF121 from Pak Sian Dong (fermented spider plant) for using as probiotics. J. Pure Appl. Microbiol. 2020; 14, 1715-22.
C Wang, T Chang, H Yang and M Cui. Antibacterial mechanism of lactic acid on physiological and morphological properties of Salmonella Enteritidis, Escherichia coli and Listeria monocytogenes. Food Contr. 2015; 47, 231-6.
SP Bangar, S Suri, M Trif and F Ozogul. Organic acids production from lactic acid bacteria: A preservation approach. Food Biosci. 2022; 46, 101615.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Walailak University
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
