In Vitro Assessment of Probiotic Properties in Lactobacillus Strains Isolated from Traditionally Fermented Thai Foods
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Published
Aug 11, 2021
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Abstract
Traditionally fermented Thai foods are good sources for Lactobacilli isolation due to these food types include a wide variety of ingredients. A total of 82 Lactobacillus strains were preliminarily isolated from Pla-Som, Pla-Duk-Ra, Pla-Pang-Dang, Kung-Som, and Nham-Hed-Nang-Fa. Their 16S rDNA sequences showed homology to L. plantarum, L. lactis, L. amylovorus, L. casei, L. acidophilus, L. farciminis, and L. graminis. Gastrointestinal tract experimental found 10 isolates that can survive at pH 2.5 and 0.9% bile salt concentration. Remaining 4 isolates of L. plantarum (LpWP48/12, LpNH48/12) and L. acidophilus (LacKS48/15, LacWP48/22) had antagonistic activity against human pathogens including Staphylococcus aureus (TISTR 746), Escherichia coli (TISTR 527), Pseudomonas aeroginosa (TISTR 357), Salmonella Typhi, and Shigella dysentery. All four isolates were resistant to streptomycin, cefotetan, nalidixic acid, vancomycin, kanamycin, and methicillin. PCR analysis revealed positive identification of the bsh, atpD and mapA genes. The virulence-related genes cylA, ace, esp and gelE were found to be absent. As a result, L. plantarum (LpWP48/12 and LpNH48/12) and L. acidophilus (LacKS48/15 and LacWP48/22) showed potential as probiotic candidates and were safe to use as starter culture.
Keywords: Lactic acid bacteria, Probiotics, Lactobacillus plantarum, Lactobacillus acidophilus, Traditionally fermented Thai food
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evaluation of Enterococcus faecium YF5 isolated from sourdough. Journal of Food Science, 78(4), 587-
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to increase safety and shelf-life of fermented foods. BioMed Research International, 2018, 1-18.
http://dx.doi.org/10.1155/2018/9361614
Botthoulath, V., Upaichit, A., & Thumarat, U. (2018). Identification and in vitro assessment of potential probiotic
characteristics and antibacterial effects of Lactobacillus plantarum subsp. plantarum SKI19, a
bacteriocinogenic strain isolated from Thai fermented pork sausage. Journal of Food Science and Technology,
55(7), 2774-2785. http://dx.doi.org/10.1007/s13197-018-3201-3
Buck, B. L., Altermann, E., Svingerud, T., & Klaenhammer, T. R. (2005). Functional analysis of putative adhesion
factors in Lactobacillus acidophilus NCFM. Applied Environmental Microbiology, 71, 8344-8351.
http://dx.doi.org/10.1128/AEM.71.12.8344-8351.2005
Chow, J. W., Thal, L. A., Perri, M. B., Vazquez, J. A., Donabedian, S. M., Clewell, D. B., & Zervos, M. J.
(1993). Plasmid-associated hemolysin and aggregation substance production contribute to virulence in
experimental enterococcal endocarditis. Antimicrobial Agent Chemotherapy, 37, 2474-2477. http://dx.
doi.org/10.1128/aac.37.11.2474
Clinical and Laboratory Standard Institute. (2009). Performance Standards for Antimicrobial Disk Susceptibility
Tests; Approved Standard (10th ed.). Wayne, Pa, USA: Clinical and Laboratory Standard Institute.
Danielsen, M., & Wind, A. (2003). Susceptibility of Lactobacillus spp. to antimicrobial agents. International Journal of Food Microbiology, 82(1), 1-11. http://dx.doi.org/ 10.1016/s0168-1605(02)00254-4
Duary, R. K., Batish, V. K., & Grover, S. (2010). Expression of the atpD gene in probiotic Lactobacillus plantarum
strains under in vitro acidic conditions using RT-qPCR. Research in Microbiology, 161(5), 399-405.
http://dx.doi.org/10.1016/j.resmic.2010.03.012
European Food Safety Authority. (2013). Scientific opinion on the maintenance of the list of QPS biological agents
intentionally added to food and feed (2013 update). The European Food Safety Authority Journal, 11(11),
1-108. http://dx.doi.org/10.2903/j.efsa.2013.3449
Ghosh, K., Ray, M., Adak, A., Halder, S. K., Das, A., Jana, A., & Mondal, K. C. (2015). Role of probiotic
Lactobacillus fermentum KKL1 in the preparation of a rice based fermented beverage. Bioresource
Technology, 188, 161-168. http://dx.doi.org/10.1016/j.biortech.2015.01.130
Gong, H. S., Meng, X. C., & Wang, H. (2010). Plantaricin MG active against Gram-negative bacteria produced
by Lactobacillus plantarum KLDS1.0391 isolated from ‘‘Jiaoke’’, a traditional fermented cream from China.
Food Control, 21, 89-96. http://dx.doi.org/10.1016/j.foodcont.2009.04.005
Gutschik, E., Moller, S., & Christensen, N. (1979). Experimental endocarditis in rabbits. 3. Significance of the
proteolytic capacity of the infecting strains of Streptococcus faecalis. Acta Pathologica et Microbiologica
Scandinavica Section B, 87, 353-362.
Handwerger, S., Pucci, M. J., Volk, K. J., Liu, J., & Lee, M. S. (1994). Vancomycin-resistant Leuconostoc
mesenteroides and Lactobacillus casei synthesize cytoplasmic peptidoglycan precursors that terminate in
lactate. Journal of Bacteriology, 176(1), 260-264. http://dx.doi.org/10.1128/jb.176.1.260-
264.1994
Hu, C. H., Ren, L. Q., Zhou, Y., & Ye, B. C. (2019). Characterization of antimicrobial activity of three
Lactobacillus plantarum strains isolated from Chinese traditional dairy food. Food Science Nutrition, 7(6),
1997-2005. http://dx.doi.org/10.1002/fsn3.1025
Jacobsen, C. N., Nielsen, V. R., Hayford, A. E., Moller, P. L., Michaelsen, K. F., Paerregaard, …
Jakobsen, M. (1999). Screening of probiotic activities of forty-seven strains of Lactobacillus
spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans.
Applied Environmental Microbiology, 65(11), 4949-4956. http://dx.doi.org/10.1128 /AEM.65.11.
4949-4956.1999
Jin, L. Z., Ho, Y. W., Abdullah, N., & Jalaludin, S. (1998). Acid and bile tolerance of Lactobacillus isolated from
chicken intestine. Letter in Applied Microbiology, 27(3), 183-185. http://dx.doi.org/10.1046/j.1472-
765x.1998.00405.x
Klayraung, S., Viernstein, H., Sirithunyalug, J., & Okonogi, S. (2008). Probiotic properties of lactobacilli isolated
from Thai traditional food. Scientia Pharmaceutica, 76(3), 485-503. http://dx.doi.org/10.3797/
scipharm.0806-11
Klein, G., Hallmann, C., Casas, I. A., Abad, J., Louwers, J., & Reuter, G. (2000). Exclusion of vanA, vanB and
vanC type glycopeptide resistance in strains of Lactobacillus reuteri and Lactobacillus rhamnosus used as
probiotics by polymerase chain reaction and hybridization methods. Journal of Applied Microbiology, 89(5),
815-824. http://dx.doi.org/10.1046/j.1365-2672.2000.01187.x
Koll, P., Mandar, R., Marcotte, H., Leibur, E., Mikelsaar, M., & Hammarstrom, L. (2008). Characterization of
oral Lactobacilli as potential probiotics for oral health. Oral Microbiology Immunity, 23(2), 139-147.
http://dx.doi.org/10.1111/j.1399-302X.2007.00402.x
Lim, S. M. (2009). Screening and characterization of probiotic lactic acid bacteria isolated from Korean fermented
foods. Journal of Microbiology and Biotechnology, 19(2), 178-186. http://dx.doi.org/10.4014/jmb.
0804.269
Lindenstrauss, A. G., Pavlovic, M., & Bringmann, A. (2011). Comparison of genotypic and phenotypic cluster
analyses of virulence determinants and possible role of CRISPR elements towards their incidence in
Enterococcus faecalis and Enterococcus faecium. Systematic and Applied Microbiology, 34(8), 553-560.
http://dx.doi.org/10.1016/j.syapm.2011.05.002
Liong, M. T., & Shah, N. P. (2005). Acid and bile tolerance and cholesterol removal ability of lactobacilli strains.
Journal of Dairy Science, 88(1), 55-66. http://dx.doi.org/10.3168/jds.S0022-0302(05)72662-X
Martı´n-Platero, A. M., Valdivia, E., Maqueda, M., & Martı´nez-Bueno, M. (2009). Characterization and safety evaluation of enterococci isolated from Spanish goats’ milk cheeses. International Journal of Food
Microbiology, 132, 24-32. http://dx.doi.org/10.1016/j.ijfoodmicro.2009.03.010
Mulaw, G., Tessema, T. S., Muleta, D., & Tesfaye, A. (2019). In Vitro Evaluation of Probiotic Properties of
Lactic Acid Bacteria Isolated from Some Traditionally Fermented Ethiopian Food Products. International
Journal of Microbiology, 7179514, 1-11. http://dx.doi.org/10.1155/2019/7179514
Neal-McKinney, J. M., Lu, X., Duong, T., Larson, C. L., Call, D. R., Shah, D. H., & Konkel, M. E. (2012).
Production of organic acids by probiotic lactobacilli can be used to reduce pathogen load in poultry. PLoS
ONE, 7(9), 43928. http://dx.doi.org/10.1371/journal.pone.0043928
O’Sullivan, L., Ross, R. P., & Hill, C. (2002). Potential of bacteriocin producing lactic acid bacteria for
improvements in food safety and quality. Biochimie, 84(5-6), 593-604. http://dx.doi.org/10.1016/
s0300-9084(02)01457-8
Pavlova, S. I., Kilic, A. O., Kilic, S. S., So, J. S., Nader-Macias, M. E., Simone, J. A., & Tao, L. (2002).
Genetic diversity of vaginal lactobacilli from women in different countries based on 16S rRNA gene
sequences. Journal of Applied Microbiology, 92(3), 451-459. http://dx.doi.org/10.1046/j.1365-
2672.2002.01547.x
Pisano, M. B., Viale, S., Conti, S., Fadda, M. E., Deplano, M., Melis, M. P., … & Cosentino, S. (2014).
Preliminary Evaluation of Probiotic Properties of Lactobacillus Strains Isolated from Sardinian Dairy
Products. BioMed Research International, 2014, 1-9. http://dx.doi.org/10.1155/2014/286390
Rodgers, S. (2008). Novel applications of live bacteria in food services: probiotics and protective cultures. Trends
Food Science and Technology, 19(4), 188-197. http://dx.doi.org/10.1016/j.tifs.2007.11.007
Sahadeva, R. P. K., Leong, S. F., K., Chua, H., Tan, C. H., Chan, H. Y., Tong, E. V., … & Chan,
H. K. (2011). Survival of commercial probiotic strains to pH and bile. International Food Research Journal,
18(4), 1515-1522.
Salminen, S., Wright, A. V., Morelli, L., Marteau, P., Brassart, D., Vos, … Mattila-Sandholm, T. (1998).
Demonstration of safety of probiotics-a review. International Journal of Food Microbiology, 44(1-2), 93-
106. http://dx.doi.org/10.1016/s0168-1605(98)00128-7
Schillinger, U., & Lücke F. K. (1989). Antibacterial activity of Lactobacillus sake isolated from meat. Applied and Environmental Microbiology, 55(8), 1901–1906. http://dx.doi.org/1901-1906.10.1128/aem.55.
8.1901-1906.1989
Shokryazdan, P., Sieo, C. C., Kalavathy, R., Liang, J. B., Alitheen, N. B., Jahromi, M. F., & Ho, Y. W. (2014).
Probiotic Potential of Lactobacillus Strains with Antimicrobial Activity against Some Human Pathogenic
Strains. BioMed Research International, 927268, 1-16. http://dx.doi.org/10.1155/2014/927268
Suskovic, J., Blazenka, K., Beganovic, J., Pavunc, A.L., Habjanic, K., & Matosic, S. (2010). Antimicrobial
activity-the most important property of probiotic and starter lactic acid bacteria. Food Technology and
Biotechnology, 48(3), 296-307.
Tan, Q., Xu, H., Aguilar, Z. P., Peng, S., Dong, S., Wang, B., … Wei, H. (2013). Safety assessment and probiotic
evaluation of Enterococcus faecium YF5 isolated from sourdough. Journal of Food Science, 78(4), 587-
593. http://dx.doi.org/10.1111/1750-3841.12079
Todorov, S. D., Botes, M., Guigas, C., Schillinger, U., Wiid, I., Wachsman, M. B., … Dicks,
L. M. T. (2008). Boza, a natural source of probiotic lactic acid bacteria. Journal of Applied Microbiology,
104, 465-477. http://dx.doi.org/10.1111/j.1365-2672.2007.03558.x
Ventura, M., Canchaya, C., Sinderen, D. V., Fitzgerald, G. F., & Zink, R. (2004). Bifidobacterium lactis DSM
10140: Identification of the atp (atpBEFHAGDC) Operon and Analysis of Its Genetic Structure,
Characteristics, and Phylogeny. Applied Environmental Microbiology, 70(5), 3110-3121. http://dx.doi.
org/10.1128/AEM.70.5.3110-3121.2004
Visessanguan, W., Plengvidha, V., Chokesajjawatee, N., & Baker, J. A. (2015). Lactic meat fermentation In
J. D. Owens (ed.). indigenous fermented foods of Southeast Asia. NY: CRC Press.
Zago, M., Fornasari, M. E., Carminati, D., Burns, P., Suarez, V., Vinderola, G., … Giraffa, G.
(2011). Characterization and probiotic potential of Lactobacillus plantarum strains isolated from cheeses.
Food Microbiology, 28, 1033-1040. http://dx.doi.org/10.1016/j.fm.2011.02.009
Zhang, B., Wang, Y., Tan, Z., Li, Z., Jiao, Z., & Huang, Q. (2016). Screening of probiotic activities of lactobacilli
strains isolated from traditional Tibetan Qula, a raw yak milk cheese. Asian-Australasian Journal of Animal
Science, 29(10), 1490-1499. http://dx.doi.org/10.5713/ajas.15.0849
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Research Articles
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How to Cite
NITIPAN, Supachai et al.
In Vitro Assessment of Probiotic Properties in Lactobacillus Strains Isolated from Traditionally Fermented Thai Foods.
Naresuan University Journal: Science and Technology (NUJST), [S.l.], v. 30, n. 2, p. 11-23, aug. 2021.
ISSN 2539-553X.
Available at: <https://www.journal.nu.ac.th/NUJST/article/view/Vol-30-No-2-2022-11-23>. Date accessed: 23 apr. 2024.
doi: https://doi.org/10.14456/nujst.2022.12.