Diversity analysis, identification, and bioprospecting of Lactic Acid Bacteria (LAB) isolated from Sumbawa horse milk
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Abstract
Abstract. Fidien KA, Manguntungi B, Sukmarini L, Mustopa AZ, Triratna L, Fatimah, Kusdianawati. 2021. Diversity analysis, identification, and bioprospecting of Lactic Acid Bacteria (LAB) isolated from Sumbawa horse milk. Biodiversitas 22: 3333-3340. Sumbawa horse milk has a probiotic potential because of the presence of Lactic Acid Bacteria (LAB). The LAB present in Sumbawa horse milk has been reported to have antimicrobial activities against pathogenic bacteria, including Staphylococcus epidermidis, Staphylococcus aureus, Escherichia coli, and Vibrio cholerae. However, the potential of LAB from Sumbawa horse milk as antioxidant and antidiabetic is still unexplored. Studies related to the diversity of indigenous bacteria in Sumbawa horse milk based on metagenomic analysis have not been widely studied either. Therefore, this study aimed to determine the diversity of species of indigenous bacteria in Sumbawa horse milk and to identify LAB bioprospecting from Sumbawa horse milk. The diversity of indigenous bacterial species was investigated by the 16S rRNA gene-targeted metagenomic approach from bacterial DNA isolated from Sumbawa horse milk. The identification of LAB was also carried out by the 16S rRNA gene identification method. LAB bioprospecting on antioxidant activity was determined using the DPPH method, while the antidiabetic activity was measured using the ?-glucosidase inhibition assay. The diversity analysis of indigenous bacteria based on 16S rRNA gene-based metagenomic revealed at least 7 phyla were relatively abundant in Sumbawa horse milk. The greatest abundance was shown by the phylum Proteobacteria (0.641%) and Firmicutes (0.327%). Enterococcus durans (39.01%) was the species that had the highest abundance in Sumbawa horse milk, followed by Lactococcus garvieae (30.13%) and Lactococcus lactis (19.85%). Moreover, based on the identification of the 16S rRNA gene, eight LAB isolates had similarities to bacterial strains, including Enterococcus faecium DSM 20477, E. faecium NBRC 100486, E. faecium ATCC 19434, E. durans 98D, E. faecalis ATCC 19433, E. faecalis NRBC 100480, Lactococcus lactis subsp. hordniae NBRC 100931 and L. garvieae JCM 10343 with similarity levels of more than 98%. In terms of LAB bioprospecting, the antioxidant assay showed the highest DPPH radical binding activity by L. garvieae L.22PR (43%). Meanwhile, the highest inhibitory activity of ?-glucosidase was shown by E. faecium G.6PR (45%).
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Abrantes, M.C., M. de Fátima Lopes, J. Kok. 2011. Impact of Manganese, Copper and Zinc Ions on the Transcriptome of the Nosocomial Pathogen Enterococcus faecalis V583. PLoS One. 6(10): 1-9.
Antara, N.S., I.N. Dibia, W.R. Aryanta. 2009. Karakterisasi Bakteri Asam Laktat yang Diisolasi Dari Susu Kuda Bima. Agritech. 29(1): 1-9.
Astuti, N.Y. 2009. Uji Aktivitas Penangkap Radikal DPPH oleh Analog Kurkumin Monoketon dan N-Heteroalifatik Monoketon. Disertasi. Univerversitas Muhammadiyah Surakarta.
Ayyash, M., B. Abu-Jdayil, P. Itsaranuwat, N. Almazrouei, E. Galiwango, Esposito, Y. Hunashal, F. Hamed, Z. Najjar. 2020. Exopolysaccharide Produced by the Potential Probiotic Lactococcus garvieae C47: Structural Characteristics, Rheological Properties, Bioactivities and Impact on Fermented Camel Milk. Food Chemistry. 333(127418).
Begley, M., C. Hill, C.G. Gahan. 2006. Bile Salt Hydrolase Activity in Probiotics. Applied and Environmental Microbiology. 72(3): 1729-1738.
Chanos, P., D.R. Williams. 2011. Anti?Listeria Bacteriocin?Producing Bacteria from Raw Ewe’s Milk in Northern Greece. Journal of Applied Microbiology. 110(3): 757-768.
Chaves-López, C., A. Serio, M. Martuscelli, A. Paparella, E. Osorio-Cadavid, G. Suzzi. 2011. Microbiological Characteristics of Kumis, a Traditional Fermented Colombian Milk, with Particular Emphasis on Enterococci Population. Food Microbiology. 28(5): 1041-1047.
Chien, L.J., C.K. Lee. 2007. Hyaluronic Acid Production by Recombinant Lactococcus lactis. Applied Microbiology and Biotechnology. 77(2): 339-346.
Dalmasso, M., D. Hennequin, C. Duc, Y. Demarigny. 2009. Influence of Backslopping on the Acidifications Curves of “Tomme” Type Cheeses Made During 10 Successive days. Journal of Food Engineering, 92(1): 50-55.
Doyle, J.J., J.L. Doyle. 1990. Isolation of Plant DNA from Fresh Tissue. Focus. 12(1):39-40
Franz, C.M., M. Huch, H. Abriouel, W. Holzapfel, A. Gálvez. 2011. Enterococci as Probiotics and Their Implications in Food Safety. International Journal of Food Microbiology. 151(2): 125-140.
Gao, Y., D. Li, S. Liu, L. Zhang. 2015. Garviecin LG34, a Novel Bacteriocin Produced by Lactococcus garvieae Isolated from Traditional Chinese Fermented Cucumber. Food Control. 50: 896-900.
Graham, C.E., M.R. Cruz, D.A. Garsin, M.C. Lorenz. 2017. Enterococcus faecalis Bacteriocin EntV Inhibits Hyphal Morphogenesis, Biofilm Formation, and Virulence of Candida albicans. Proceedings of the National Academy of Sciences. 114(17): 4507-4512.
Graham, K., R. Rea, P. Simpson, H. Stack. 2019. Enterococcus faecalis Milk Fermentates Display Antioxidant Properties and Inhibitory Activity Towards Key Enzymes Linked to Hypertension and Hyperglycaemia. Journal of Functional Foods. 58: 292-300.
Handelsman, J. 2004. Metagenomics: Application of Genomics to Uncultured Microorganisms. Microbiology and Molecular Biology Reviews. 68(4): 669-685.
Jatmiko, Y..,I. Mustafa, T. Ardyati. 2019. Profile of Microbial Community of Naturally Fermented Sumbawa Mare’s Milk Using Next-Generation Sequencing. Berkala Penelitian hayati. 24(2): 65-69
Kodali, V.P., R. Sen. 2008. Antioxidant and Free Radical Scavenging Activities of an Exopolysaccharide from a Probiotic Bacterium. Biotechnology Journal: Healthcare Nutrition Technology. 3(2): 245-251.
Kusdianawati, A.Z. Mustopa, Fatimah, B.R. Budiarto. 2020. Genetic Diversity of Lactic Acid Bacteria from Sumbawa Horse Milk, Indonesia. Biodiversitas. 21(7): 3225-3233.
Laily, I.N., R. Utami, E. Widowati. 2013. Isolasi dan Karakterisasi Bakteri Asam Laktat Penghasil Riboflavin dari Produk Fermentasi Sawi Asin. Jurnal Aplikasi Teknologi Pangan. 2(4): 179-184.
Lacroix, I.M., E.C. Li-Chan. 2013. Inhibition of Dipeptidyl Peptidase (DPP)-IV and ?-Glucosidase Activities by Pepsin-Treated Whey Proteins. Journal of Agricultural and Food Chemistry. 61(31): 7500-7506.
Li, B., S.E. Evivie, D. Jin, Y. Meng, N. Li, F. Yan, G. Huo, F. Liu. 2018. Complete Genome Sequence of Enterococcus durans KLDS6. 0933, a Potential Probiotic Strain with High Cholesterol Removal Ability. Gut Pathogens. 10(32): 1-6.
Liu, J., J. Zhou, L. Wang, Z. Ma, G. Zhao, Z. Ge, H. Zhu, J. Qiao. 2017. Improving Nitrogen Source Utilization from Defatted Soybean Meal for Nisin Production by Enhancing Proteolytic Function of Lactococcus lactis F44. Scientific Reports. 7(1): 1-13.
Manguntungi, B., A.S. Perkasa, Kusdianawati, H.P. Hastuti, Yulianti dan A. Muhamad. 2018. Isolasi Bakteri Asam Laktat dari Susu Kuda Liar dan Potensi Antibakteri pada Susu Kuda Liar Sumbawa. Biota: Jurnal Ilmiah Ilmu-Ilmu Hayati. 3(2): 62-69.
Manguntungi, A.B., DS. Saputri, A.Z. Mustopa, N. Ekawati, M. Nurfatwa, A. Prastyowati, S. Irawan, L.R. Vanggy, K.A. Fidien. 2020. Antidiabetic, Antioxidants and Antibacterial Activities of Lactic Acid Bacteria (LAB) from Masin (Fermented Sauced from Sumbawa, West Nusa Tenggara, Indonesia). Annales Bogorienses. 24(1): 27-34.
Mehanna, N.S., N.F. Tawfik, M.M. Salem, B.A. Effat, D.A. Gad El-Rab. 2013. Assessment of Potential Probiotic Bacteria Isolated from Breast Milk. Middle-East Journal of Scientific Research. 14(3): 354-360.
Muganga, L., X. Liu, F. Tian, J. Zhao, H. Zhang,W. Chen. 2015. Screening for Lactic Acid Bacteria Based on Antihyperglycaemic and Probiotic Potential and Application in Synbiotic Set Yoghurt. Journal of Functional Foods. 16: 125-136.
Ng, Z.J., M.A. Zarin, C.K. Lee, P. Phapugrangkul, J.S. Tan. 2020. Isolation and Characterization of Enterococcus faecium DSM 20477 with Ability to Secrete Antimicrobial Substance for the Inhibition of Oral Pathogen Streptococcus mutans UKMCC 1019. Archives of Oral Biology. 110:104617.
Nimnoi, P., N. Pongsilp. 2020. Marine Bacterial Communities in the Upper Gulf of Thailand Assessed by Illumina Next-Generation Sequencing Platform. BMC Microbiology. 20(1): 1-11.
Noreen, N., W.Y. Hooi, A. Baradaran, M. Rosfarizan, C.C. Sieo, M.I. Rosli, K. Yusoff, A.R. Raha. 2011. Lactococcus lactis M4, a Potential Host for the Expression of Heterologous Proteins. Microbial Cell Factories. 10(1): 1-10.
Nuraida, L. 2015. A Review: Health Promoting Lactic Acid Bacteria In traditional Indonesian Fermented Foods. Food Science and Human Wellness. 4(1): 47-55.
Pan, D., X. Mei. 2010. Antioxidant Activity of an Exopolysaccharide Purified from Lactococcus lactis subsp. lactis 12. Carbohydrate Polymers. 80(3): 908-914.
Patten, D.A., A.P. Laws. 2015. Lactobacillus-Produced Exopolysaccharides and Their Potential Health Benefits: A Review. Beneficial Microbes. 6(4): 457-471.
Pratama, Y., P.R. Sarjono, N.S. Mulyani. 2015. Skrining Metabolit Sekunder Bakteri Endofit yang Berfungsi sebagai Antidiabetes dari Daun Mimba (Azadirachtaindica). Jurnal Kimia dan Aplikasi Sains. 18(2): 73-78.
Ramchandran, L., N.P. Shah. 2008. Proteolytic Profiles and Angiotensin?I Converting Enzyme and ??Glucosidase Inhibitory Activities of Selected Lactic Acid Bacteria. Journal of Food Science. 73(2): 75-81.
Ramchandran, L., N.P. Shah. 2009. Effect of Exopolysaccharides and Inulin on the Proteolytic, Angiotensin-I-Converting Enzyme-and a-Glucosidase Inhibitory Activities as well as on Textural and Rheological Properties of Lowfat Yogurt During Refrigerated Storage. Dairy Science and Technology. 89(1): 583-600.
Rattanachaikunsopon, P., P. Phumkhachorn. 2010. Lactic Acid Bacteria: Their Antimicrobial Compounds and Their Uses in Food Production. Annals of Biological Research. 1(4): 218-228.
Reller, L.B., M.P. Weinstein, C.A. Petti. 2007. Detection and Identification of Microorganisms by Gene Amplification and Sequencing. Clinical Infectious Diseases. 44(8): 1108-1114.
Reni, S., S. Sumarno, E. Widjajanto. 2013. Susu Kuda Sumbawa Meningkatkan Respon Imun Seluler Makrofag Peritoneal Mencit terhadap Salmonella typhimurium. Jurnal Kedokteran Brawijaya. 26(1): 14-19.
Ridho, E.A. 2013. Uji Aktivitas Antioksidan Ekstrak N-heksan Buah Lakum (Cayratia trifolia) dengan Metode DPPH (2, 2-difenil-1-pikrilhidrazil). Doctoral Dissertation. Tanjungpura University.
Seo, B.J., V.K. Bajpai, I.A. Rather, Y.H. Park. 2015. Partially Purified Exopolysaccharide from Lactobacillus plantarum YML009 with Total Pphenolic Content, Antioxidant and Free Radical Scavenging Efficacy. Indian Journal of Pharmaceutical Education and Research. 49(4): 282-292.
Setyowati, E.P., F.N. Laili, S. Iravati. 2012. Sumbawa Horse Milk Typical Indonesian Antibacterial Cosmetic Ingredients Against Acne (Staphylococcus Epidermidis). Traditional Medicine Journal. 19(2): 74-79.
Shimada, K., K. Fujikawa, K. Yahara, T. Nakamura. 1992. Antioxidative Properties of Xanthan on the Autoxidation of Soybean Oil in Cyclodextrin Emulsion. Journal of Agricultural and Food Chemistry, 40(6): 945-948.
Sujaya, I.N., N.P.D. Aryantini, N.W. Nursini, C.I.D. Cakrawati, N.L.M.E. Juliasari, N.M.U. Dwipayanti, Y. Ramona. 2012. Eksopolisakarida dari Lactobacillus sp. Isolat Susu Kuda Sumbawa dan Potensinya sebagai Prebiotik. Jurnal Veteriner. 13(2): 136-144.
Sujaya, I.N., I.M.U Dwipayanti, N.L.P. Suariani, N.P. Widarini, K.A. Nocianitri, N.W. Nursini. 2008a. Potensi Lactobacillus spp. Isolay Susu Kuda Sumbawa Sebagai Probiotik. Jurnal Veteriner. 9(1): 33-40.
Sujaya, N., Y. Ramona, N.P. Widarini, N.P. Suariani, N.M.U. Dwipayanti, K.A. Nocianitri, N.W. Nursini. 2008b. Isolasi dan Karakterisasi Bakteri Asam Laktat dari Susu Kuda Sumbawa. Jurnal Veteriner. 9(2): 52-59.
Tagliazucchi, D., S. Martini, L. Solieri. 2019. Bioprospecting for Bioactive Peptide Production by Lactic Acid Bacteria Isolated from Fermented Dairy Food. Fermentation. 5(4): 96.
Tejedor, J.L., A.I. Vela, A. Gibello, A. Casamayor, L. Domínguez, J.F. Fernández-Garayzábal. 2011. A Genetic Comparison of Pig, Cow and Trout Isolates of Lactococcus garvieae by PFGE analysis. Letter in Applied Microbiology. 53(1): 614–619.
Teng, F., S.S.D. Nair, P. Zhu, S. Li, S. Huang, X: Li, J. Xu, F. Yang. 2018. Impact of DNA Extraction Method and Targeted 16S-rRNA Hypervariable Region on Oral Microbiota Profiling. Scientific Reports. 8(1): 1-12.
Todorov, S. D., M. Wachsman, E. Tomé, X. Dousset, M.T. Destro, L.M.T. Dicks, D.G.M. Franco Drider, D. 2010. Characterisation of an Antiviral Pediocin-Like Bacteriocin Produced by Enterococcus faecium. Food Microbiology. 27(7): 869-879.
Tormo, H., D.A.H. Lekhal, C. Roques. 2015. Phenotypic and Genotypic Characterization of Lactic Acid Bacteria Isolated from Raw Goat Milk and Effect of Farming Practices on the Dominant Species of Lactic Acid Bacteria. International Journal of Food Microbiology. 210: 9-15.
Tosukhowong, A., T. Zendo, W. Visessanguan, S. Roytrakul, L. Pumpuang, J. Jaresitthikunchai, K. Sonomoto. 2012. Garvieacin Q, a Novel Class II Bacteriocin from Lactococcus garvieae BCC 43578. Applied and Environmental Microbiology. 78(5): 1619-1623.
Volzing, K., J. Borrero, M.J. Sadowsky, Y.N. Kaznessis. 2013. Antimicrobial Peptides Targeting Gram-Negative Pathogens, Produced and Delivered by Lactic Acid Bacteria. ACS . Synthetic Biology. 2(11): 643-650.
Ward, T.L., S. Hosid, I. Ioshikhes, I. Altosaar. 2013. Human Milk Metagenome: A Functional Capacity Analysis. BMC Microbiology. 13(1): 1-12.
Wyszy?ska, A., P. Kobierecka, J. Bardowski, E.K. Jagusztyn-Krynicka. 2015. Lactic Acid Bacteria: 20 Years Exploring Their Potential as Live Vectors for Mucosal Vaccination. Applied Microbiology and Biotechnology. 99(7): 2967-2977.
Yazdankhah, S.P., D. Grahek-Ogden, K.F. Eckner, G. Kapperud, J.F. Lassen, J. Narvhus, T. Nesbakken, L. Robetson, J.T. Rosnes, T. Skjerdal, L. Vold, E. Skjerve, Y. Wasteson. 2016. Risk Assessment of Lactococcus lactis W58 Used as "Other Substances". Opinion of the Panel on Biological Hazards of the Norwegian Scientific Committee for Food Safety. VKM Report. 28: 1-20.
Zahratunnisa, N., B. Elya, A. Noviani. 2017. Inhibition of Alpha-Glucosidase and Antioxidant Test of Stem Bark Extracts of Garcinia fruticosa Lauterb. Pharmacognosy Journal. 9(2): 273-275.
Zhang, F., Z. Wang, F. Lei, B. Wang, S. Jiang, Q. Peng, J, ZhangY. Shao. 2017b. Bacterial Diversity in Goat Milk from the Guanzhong Area of China. Journal of Dairy Science. 100(10): 7812-7824.
Zhang, J., X. Zhao, Y. Jiang, W. Zhao, T. Guo, Cao, J. Teng, X. Hao, J. Hao, Z. Yang. 2017a. Antioxidant Status and Gut Microbiota Change in an Aging Mouse model as influenced by exopolysaccharide produced by Lactobacillus plantarum YW11 isolated from Tibetan kefir. Journal of Dairy Science. 100(8): 6025-6041.
Zhao, Q., B. Dong, J. Chen, B. Zhao, X. Wang, L. Wang, S. Zha, Y. Wang, J. Zhang, Y. Wang. 2015. Effect of Drying Methods on Physicochemical Properties and Antioxidant Activities of Wolfberry (Lycium barbarum) Polysaccharide. Carbohydrate Polymers. 127(1): 176-181.
Zhou, Y., Y. Cui, X. Qu. 2019. Exopolysaccharides of Lactic Acid Bacteria: Structure, Bioactivity and Associations: A Review. Carbohydrate Polymers. 207: 317-332.
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