Genomic insight of two indigenous probiotics Lactobacillus plantarum Dad-13 and Lactobacillus plantarum Mut-7 from different origins of Indonesian fermented foods

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DIAN ANGGRAINI SUROTO
PRATAMA NUR HASAN
ENDANG SUTRISWATI RAHAYU

Abstract

Abstract. Suroto DA, Hasan PN, Rahayu ES. 2021. Genomic insight of two indigenous probiotics Lactobacillus plantarum Dad-13 and Lactobacillus plantarum Mut-7 from different origins of Indonesian fermented foods. Biodiversitas 22: 5491-5500. Lactobacillus plantarum Dad-13 and Lactobacillus plantarum Mut-7 are probiotics isolated from traditional fermented foods. In the present study two strains of L. plantarum were sequenced using Illumina NovaSeq PE150 platform and in silico analysis was performed using RAST webserver to unravel the functional metabolic between two strains. The L. plantarum Dad-13 and Mut-7 genome sizes were 3.25 and 3.98 Mb with GC content of them being almost similar i.e. 44.4 and 44.3%, respectively. Two lactobacilli also had some differences in their metabolic genes, particularly in carbohydrate subsystem. L. plantarum Mut-7 had genes related to the metabolisms of plant cell wall components such as dextrin, arabinose, xylose indicated the adaptation to their environmental origins (fermented dried cassava), while those genes were not observed in L. plantarum Dad-13 which was isolated from fermented buffalo’s milk (dadih). Further analysis using BAGEL4 webserver exhibited their different potential to synthesize bacteriocins, L. plantarum Dad-13 was predicted to produce more types of bacteriocins than L. plantarum Mut-7. This investigation revealed that L. plantarum Dad-13 and L. plantarum Mut-7 have a great potential related with their properties as probiotics.

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References
Ahaddin AY, Budiarti S, Mustopa AZ, Darusman HS, Triratna L. 2021. Short Communication: Acute toxicity study of plantaricin from Lactobacillus plantarum S34 and its antibacterial activity. Biodiversitas 22: 227-232. https://doi.org/10.13057/biodiv/d220128
Albayrak ,Ç.B., and Duran, M. (2021). Isolation and characterization of aroma producing lactic acid bacteria from artisanal white cheese for multifunctional properties. LWT - Food Science and Technology 150 (2021) 112053. https://doi.org/10.1016/j.lwt. 2021.112053
Arasu M.V., Al-Dhabi, N.A., Ilavenil,S., Choi, K.C., Srigopalram, S .(2016). In vitro importance of probiotic Lactobacillus plantarum related to medical field. Saudi Journal of Biological Sciences,23, S6–S10. http://dx.doi.org/10.1016/j.sjbs.2015.09.022
Ashaolu, T.J, and Reale, A. (2020). A Holistic Review on Euro-Asian Lactic Acid Bacteria Fermented Cereals and Vegetables. Microorganisms 2020, 8, 1176.https://doi.org/10.3390/microorganisms8081176.
Austin, M. B., & Noel, J. P. (2003). The chalcone synthase superfamily of type III polyketide synthases. Natural product reports, 20(1), 79–110. https://doi.org/10.1039/b100917f
Ayivi,R.D., Gyawali,R., Krastanov, R., Aljaloud, S.O.,Worku, M.,Tahergorabi R., da Silva, R.C., and Ibrahim, S.A. (2020). Lactic Acid Bacteria: Food Safety and Human Health Applications. Dairy, 1, 202–232. https://doi.org/10.3390/dairy1030015
Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S., Prjibelski, A. D., Pyshkin, A. V., Sirotkin, A. V., Vyahhi, N., Tesler, G., Alekseyev, M. A., & Pevzner, P. A. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of computational biology : a journal of computational molecular cell biology, 19(5), 455–477. https://doi.org/10.1089/cmb.2012.0021
Barbosa, J.; Albano, H.; Silva, B.; Almeida, M.H.; Nogueira, T.; Teixeira, P. Characterization of a Lactiplantibacillus plantarum R23 Isolated from Arugula by Whole-Genome Sequencing and Its Bacteriocin Production Ability. Int. J. Environ. Res. Public Health 2021, 18, 5515. https://doi.org/10.3390/ ijerph18115515
Behera,S.S., Ray ,R. C., and Zdolec, N. (2018). Lactobacillus plantarum with Functional Properties: An Approach to Increase Safety and Shelf-Life of Fermented Foods. BioMed Research International Volume 2018, Article ID 9361614 https://doi.org/10.1155/2018/9361614
Bengtsson, T., Selegård, R., Musa, A. et al. Plantaricin NC8 ?? exerts potent antimicrobial activity against Staphylococcus spp. and enhances the effects of antibiotics. Sci Rep 10, 3580 (2020). https://doi.org/10.1038/s41598-020-60570-w
Bermudez-Brito, M.,Plaza-Díaz, J., Muñoz-Quezada , S., Gómez-Llorente, C., Gil, A.(2012). Probiotic Mechanisms of Action. Ann Nutr Metab. ;61:160–174. https://doi.org/10.1159/000342079
Blin, K., Shaw, S., Kloosterman, A.M, Charlop-Powers, Z., van Wezel, G. P., Medema, M.H.,Weber, T. (2021). antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Research, 49 (W1) pp. W29–W35, https://doi.org/10.1093/nar/gkab335
Butorac, K., Bani?, M., Novak, J., Leboš Pavunc, A., Uroi?, K., Durgo, K., Oršoli?, N., Kukolj, M., Radovi?, S., Scalabrin, S., Žu?ko, J., Star?evi?, A., Šuškovi?, J., & Kos, B. (2020). The functional capacity of plantaricin-producing Lactobacillus plantarum SF9C and S-layer-carrying Lactobacillus brevis SF9B to withstand gastrointestinal transit. Microbial cell factories, 19(1), 106. https://doi.org/10.1186/s12934-020-01365-6
Chapot-Chartier, M. P., & Kulakauskas, S. (2014). Cell wall structure and function in lactic acid bacteria. Microbial cell factories, 13 Suppl 1(Suppl 1), S9. https://doi.org/10.1186/1475-2859-13-S1-S9
Deem M. W. (2020). CRISPR recognizes as many phage types as possible without overwhelming the Cas machinery. Proceedings of the National Academy of Sciences of the United States of America, 117(14), 7550–7552. https://doi.org/10.1073/pnas.2002746117
Fe?kaninováa, A., Koš?ováb, J., Mudro?ováb,D.,Schusterováb, P.,Maruš?ákováb, I.C., Popelkaa,P. (2019). Aquaculture, 506, 294–301. https://doi.org/10.1016/j.aquaculture.2019.03.026.
Fhoula, I., Najjari, A.,Turki,Y., Jaballah, S., Boudabous, A., and Ouzar, H. (2013). Diversity and Antimicrobial Properties of Lactic Acid Bacteria Isolated from Rhizosphere of Olive Trees and Desert Truffles of Tunisia. BioMed Research Internationalvol. 2013, Article ID 405708. https://doi.org/10.1155/2013/405708
Fitrianingthias, R. R. D. R., Utami, T., Yanti, R., Widada, J., & Rahayu, E. S. (2018). Consumption of Indigenous Probiotic Lactobacillus plantarum Mut-7 Powder and Fecal Population of Lactobacillus, Bifidobacterium, Clostridium, and Short Chain Fatty Acids. International Journal of Probiotics and Prebiotics Vol., 13(4), 143–150.
Garcia-Vello, P., Sharma, G., Speciale, I., Molinaro, A., Im, S. H., & De Castro, C. (2020). Structural features and immunological perception of the cell surface glycans of Lactobacillus plantarum: a novel rhamnose-rich polysaccharide and teichoic acids. Carbohydrate polymers, 233, 115857. https://doi.org/10.1016/j.carbpol.2020.115857
Gaspar, C., Donders, G. G., Palmeira-de-Oliveira, R., Queiroz, J. A., Tomaz, C., Martinez-de-Oliveira, J., & Palmeira-de-Oliveira, A. (2018). Bacteriocin production of the probiotic Lactobacillus acidophilus KS400. AMB Express, 8(1), 153. https://doi.org/10.1186/s13568-018-0679-z
Gupta, S.,Mohanty, U., Majumdar, R.K. (2021). Isolation and characterization of lactic acid bacteria from traditional fermented fish product Shidal of India with reference to their probiotic potential. LWT - Food Science and Technology 146 (2021) 111641. http://doi.org/10.1016/j.lwt.2021.111641
He, Y., Wang, M., Liu, M., Huang, L., Liu, C., Zhang, X., Yi, H., Cheng, A., Zhu, D., Yang, Q., Wu, Y., Zhao, X., Chen, S., Jia, R., Zhang, S., Liu, Y., Yu, Y., & Zhang, L. (2018). Cas1 and Cas2 From the Type II-C CRISPR-Cas System of Riemerella anatipestifer Are Required for Spacer Acquisition. Frontiers in cellular and infection microbiology, 8, 195. https://doi.org/10.3389/fcimb.2018.00195
Ikhsani AY, Riftyan E, Safitri RA, Marsono Y, Utami T, Widada J, Rahayu ES. Safety Assessment of Indigenous Probiotic Strain Lactobacillus plantarum Mut-7 using sprague dawley Rats as a model. Am J Pharmacol. 2020; 15: 7-16.
Kareem, R. A and Razavi , S.(2019). Plantaricin bacteriocins?: As safe alternative antimicrobial peptides in food preservation — A review. Journal of Food Safety, 40 pp 1-12. https://doi.org/10.1111/jfs.12735
Kim, E., Chang, H. C., & Kim, H. Y. (2020). Complete Genome Sequence of Lactobacillus plantarum EM, A Putative Probiotic Strain with the Cholesterol-Lowering Effect and Antimicrobial Activity. Current microbiology, 77(8), 1871–1882. https://doi.org/10.1007/s00284-020-02000-8
Le,B., and Yang, S.H., (2018)Efficacy of Lactobacillus plantarum in prevention of inflammatory bowel disease. Toxicology Reports, 5, 314–317. https://doi.org/10.1016/j.toxrep.2018.02.007
Li.M., Wang, Y., Cui, H., Li, Y., Sun Y., and Qiu, H. (2020). Characterization of Lactic Acid Bacteria Isolated From the Gastrointestinal Tract of a Wild Boar as Potential Probiotics. Front. Vet. Sci. 7:49. https://doi.org/10.3389/fvets.2020.00049
Lim, H. J., Lee, E., Yoon, Y., Chua, B., & Son, A. (2015). Portable lysis apparatus for rapid single-step DNA extraction of Bacillus subtilis. 379–387. https://doi.org/10.1111/jam.13011
Lim, Y. P., Go, M. K., & Yew, W. S. (2016). Exploiting the Biosynthetic Potential of Type III Polyketide Synthases. Molecules (Basel, Switzerland), 21(6), 806. https://doi.org/10.3390/molecules21060806
Lin S-H, Liao Y-C (2013) CISA: Contig Integrator for Sequence Assembly of Bacterial Genomes. PLoS ONE 8(3): e60843. https://doi.org/10.1371/journal.pone.0060843
Linares, D.M, Gómez, C., Renes, E.,Fresno. J.M., Tornadijo, M.E., Ross, R.P., and Stanton,C., (2017) .Lactic Acid Bacteria and Bifidobacteria with Potential to Design Natural Biofunctional Health-Promoting Dairy Foods. Front. Microbiol. 8:846.
Luo, R., Liu, B., Xie, Y., Li, Z., Huang, W., Yuan, J., He, G., Chen, Y., Pan, Q., Liu, Y., Tang, J., Wu, G., Zhang, H., Shi, Y., Liu, Y., Yu, C., Wang, B., Lu, Y., Han, C., Cheung, D. W., … Wang, J. (2012). SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler. GigaScience, 1(1), 18. https://doi.org/10.1186/2047-217X-1-18
Medjaoui, I., Rahmani, B., Talhi, M.,Mahammi, F.Z., Moghti, F., Z.,Mehtara, N., and Gaouar, S.B.S.(2016). Isolation and Characterization of Lactic Acid Bacteria from Human Milk and Newborn Feces. J. Pure and Applied Microbilogy 2016. Vol. 10(4), p. 2613-2620. http://dx.doi.org/10.22207/JPAM.10.4.17
Nuraida, L.(2015).A review: Health promoting lactic acid bacteria in traditional Indonesian fermented foods,Food Science and Human Wellness,Volume 4, Issue 2,Pages 47-55, https://doi.org/10.1016/j.fshw.2015.06.001
Overbeek, R., Olson, R., Pusch, G. D., Olsen, G. J., D.avis, J. J., Disz, T., Edwards, R. A., Gerdes, S., Parrello, B., Shukla, M., Vonstein, V., Wattam, A. R., Xia, F., & Stevens, R. (2014). The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic acids research, 42, D206–D214. https://doi.org/10.1093/nar/gkt1226
Prasirtsaka, B.,Tanasupawatb, S., Boonsombatc, R.,Kodamac, K., and Thongchulc, K.(2013). Characterization of lactic acid producing bacteria from Thai sources. Journal of Applied Pharmaceutical Science Vol. 3 (01), 033-038. https://doi.org/10.7324/JAPS.2013.30107
Rahayu, E.S., Rusdan, I.H., Athennia, A., Kamil, R.Z, Pramesi, P.C., Marsono, Y., Utami. T, Widada, J. Safety Assessment of Indigenous Probiotic Strain Lactobacillus plantarum Dad-13 Isolated from Dadih Using Sprague Dawley Rats as a Model. Am J Pharmacol. 2019; 14: 38-47.
Rahayu, E. S. (2003). Lactic Acid Bacteria in Fermented-Foods of Indonesia Origin. Agritech, 23(2),8. https://doi.org/10.22146/agritech.13515
Rahayu, E. S., Cahyanto, M. ., Windiarti, L., Sutriyanto, J., Kandarina, T., & Utami, T. (2016). Effects of Consumption of Fermented Milk Containing Indigenous Probiotic Lactobacillus plantarum Dad-13 on the Fecal Microbiota of Healthy Indonesian Volunteers. International Journal of Probiotics and Prebiotics, 11(2), 91–98.
Rahayu, E. S., Yogeswara, A., Mariyatun, Windiarti, L., Utami, T., & Watanabe, K. (2016). Molecular characteristics of indigenous probiotic strains from Indonesia. International Journal of Probiotics and Prebiotics, 11(2), 109–116.
Ramu, R., Shirahatti, P. S., Devi, A. T., Prasad, A., J., K., M. S., L., F., Z., B. L., D., & M. N., N. P. (2015). Bacteriocins and Their Applications in Food Preservation. Critical Reviews in Food Science and Nutrition, July, 00–00. https://doi.org/10.1080/10408398.2015.1020918
Richter, C., Chang, J. T., & Fineran, P. C. (2012). Function and regulation of clustered regularly interspaced short palindromic repeats (CRISPR) / CRISPR associated (Cas) systems. Viruses, 4(10), 2291–2311. https://doi.org/10.3390/v4102291
Rodrigo-Torres, L., Yépez, A., Aznar, R., & Arahal, D. R. (2019). Genomic Insights Into Five Strains of Lactobacillus plantarum With Biotechnological Potential Isolated From chicha, a Traditional Maize-Based Fermented Beverage From Northwestern Argentina. Frontiers in microbiology, 10, 2232. https://doi.org/10.3389/fmicb.2019.02232
Selegård, R., Musa, A., Nyström, P., Aili, D., Bengtsson, T., & Khalaf, H. (2019). Plantaricins markedly enhance the effects of traditional antibiotics against Staphylococcus epidermidis. Future microbiology, 14(3), 195–205. https://doi.org/10.2217/fmb-2018-0285
Sentürk, M., Ercan, F., & Yalcin, S. (2020). The secondary metabolites produced by Lactobacillus plantarum downregulate BCL-2 and BUFFY genes on breast cancer cell line and model organism Drosophila melanogaster: molecular docking approach. Cancer chemotherapy and pharmacology, 85(1), 33–45. https://doi.org/10.1007/s00280-019-03978-0
Shiroda, M., and Manning, S.D.(2020). Lactobacillus strains vary in their ability to interact with human endometrial stromal cells. PLoS ONE 15(9): e0238993. https://doi.org/10.1371/journal. pone.0238993
Sica, M.G., Olivera,N.L., Brugnoni, L.I., Marucci, P.L., Cazorla, A.C.L., and Cubitto, M.C.(2010). Isolation, identification and antimicrobial activity of lactic acid bacteria from the Bahía Blanca Estuary. Revista de Biología Marina y Oceanografía Vol. 45, Nº3: 389-397.
Siezen, R. J., Starrenburg, M. J., Boekhorst, J., Renckens, B., Molenaar, D., & van Hylckama Vlieg, J. E. (2008). Genome-scale genotype-phenotype matching of two Lactococcus lactis isolates from plants identifies mechanisms of adaptation to the plant niche. Applied and environmental microbiology, 74(2), 424–436. https://doi.org/10.1128/AEM.01850-07
Silva, L.A., Lopes Neto, J.H.P. & Cardarelli, H.R.(2019) Exopolysaccharides produced by Lactobacillus plantarum: technological properties, biological activity, and potential application in the food industry. Ann Microbiol 69, 321–328. https://doi.org/10.1007/s13213-019-01456-9
Simpson, J. T., Wong, K., Jackman, S. D., Schein, J. E., Jones, S. J., & Birol, I. (2009). ABySS: a parallel assembler for short read sequence data. Genome research, 19(6), 1117–1123. https://doi.org/10.1101/gr.089532.108
Sophatha, B., Piwat, S.,Teanpaisan, R. (2020). Adhesion, anti?adhesion and aggregation properties relating to surface charges of selected Lactobacillus strains: study in Caco?2 and H357 cells. Archives of Microbiology (2020) 202:1349–1357 https://doi.org/10.1007/s00203-020-01846-7
Syaputri, Y. and Iwahashi, H. (2020). Characteristics of Heterologous Plantaricin from Lactobacillus plantarum and its Future in Food Preservation. Reviews in Agricultural Science, 8,124-137. https://doi.org/10.7831/ras.8.0_124
Tamang, J. P., Watanabe, K., & Holzapfel, W. H. (2016). Review: Diversity of Microorganisms in Global Fermented Foods and Beverages. Frontiers in microbiology, 7, 377. https://doi.org/10.3389/fmicb.2016.00377
Tarrah, A., Pakroo, S., Corich, V., & Giacomini, A. (2020). Whole-genome sequence and comparative genome analysis of Lactobacillus paracasei DTA93, a promising probiotic lactic acid bacterium. Archives of microbiology, 202(7), 1997–2003. https://doi.org/10.1007/s00203-020-01883-2
Todorov, S.D., Holzapfel, W. & Nero, L.A. (2016). Characterization of a novel bacteriocin produced by Lactobacillus plantarum ST8SH and some aspects of its mode of action. Ann Microbiol 66, 949–962 https://doi.org/10.1007/s13213-015-1180-4
Trush, E. A., Poluektova, E. A.,Beniashvilli, A.G., Shifrin, O.S., .Poluektov, Y.M., Ivashkin, V. T. (2020). The Evolution of Human Probiotics: Challenges and Prospects. Probiotics and Antimicrobial Proteins :12:1291–1299 https://doi.org/10.1007/s12602-019-09628-4
Valan Arasu, M., Jung, M. W., Ilavenil, S., Jane, M., Kim, D. H., Lee, K. D., Park, H. S., Hur, T. Y., Choi, G. J., Lim, Y. C., Al-Dhabi, N. A., & Choi, K. C. (2013). Isolation and characterization of antifungal compound from Lactobacillus plantarum KCC-10 from forage silage with potential beneficial properties. Journal of applied microbiology, 115(5), 1172–1185. https://doi.org/10.1111/jam.12319
van Heel, A. J., de Jong, A., Song, C., Viel, J. H., Kok, J., & Kuipers, O. P. (2018). BAGEL4: a user-friendly web server to thoroughly mine RiPPs and bacteriocins. Nucleic acids research, 46(W1), W278–W281. https://doi.org/10.1093/nar/gky383.
Vinogradov, E., Sadovskaya, I., Grard, T., & Chapot-Chartier, M. P. (2016). Structural studies of the rhamnose-rich cell wall polysaccharide of Lactobacillus casei BL23. Carbohydrate research, 435, 156–161. https://doi.org/10.1016/j.carres.2016.10.002
Waki, T., Mameda, R., Nakano, T., Yamada, S., Terashita, M., Ito, K., Tenma, N., Li, Y., Fujino, N., Uno, K., Yamashita, S., Aoki, Y., Denessiouk, K., Kawai, Y., Sugawara, S., Saito, K., Yonekura-Sakakibara, K., Morita, Y., Hoshino, A., Takahashi, S., Nakayama, T. (2020). A conserved strategy of chalcone isomerase-like protein to rectify promiscuous chalcone synthase specificity. Nature communications, 11(1), 870. https://doi.org/10.1038/s41467-020-14558-9
Wang, Y.,Yuxuan, Q., Qing, X., Ying, Z.,Jinrong,H., Pinglan, L (2018).Purification and Characterization of Plantaricin LPL-1, a Novel Class IIa Bacteriocin Produced by Lactobacillus plantarum LPL-1 Isolated From Fermented Fish. Frontiers in Microbiology ,9, 2276 https://doi.org/10.3389/fmicb.2018.02276
Wen, L.S., Philip,K., Ajam,N.(2016). Purification, characterization and mode of action of plantaricin K25 produced by Lactobacillus plantarum,Food Control,Volume 60,Pages 430-439. https://doi.org/10.1016/j.foodcont.2015.08.010.
Xiao, Y., Zhao, J., Zhang, H., Zhai, Q., & Chen, W. (2021). Mining genome traits that determine the different gut colonization potential of Lactobacillus and Bifidobacterium species. Microbial genomics, 7(6), 10.1099/mgen.0.000581. https://doi.org/10.1099/mgen.0.000581
Xu, M., Guo,L., Gu, S., Wang,O., Zhang, R., Peters, B.A.,Fan, G., Liu, X., Xu,X.,Deng, L., Zhang,Y. (2020) TGS-GapCloser: A fast and accurate gap closer for large genomes with low coverage of error-prone long reads, GigaScience, 9, giaa094. https://doi.org/10.1093/gigascience/giaa094.
Yu, J., Ahn, S., Kim, K., Caetano-Anolles, K., Lee, C., Kang, J., Cho, K., Yoon, S. H., Kang, D. K., & Kim, H. (2017). Comparative Genomic Analysis of Lactobacillus plantarum GB-LP1 Isolated from Traditional Korean Fermented Food. Journal of microbiology and biotechnology, 27(8), 1419–1427. https://doi.org/10.4014/jmb.1704.04005.
Zhang, N., Li, C.,Niu, Z., Kang,H., Wang,M., Zhanga, B., and Tian, H. (2020). Colonization and immunoregulation of Lactobacillus plantarum BF_15, a novel probiotic strain from the feces of breast-fed infants. Food Funct.,11, 3156-3166. https://doi.org/10.1039/C9FO02745A.
Zhao, S., Han, J., Bie, X., Lu, Z., Zhang, C., & Lv, F. (2016). Purification and Characterization of Plantaricin JLA-9: A Novel Bacteriocin against Bacillus spp. Produced by Lactobacillus plantarum JLA-9 from Suan-Tsai, a Traditional Chinese Fermented Cabbage. Journal of agricultural and food chemistry, 64(13), 2754–2764. https://doi.org/10.1021/acs.jafc.5b05717
Zhu, X., Zhao, Y., Sun, Y., & Gu, Q. (2014). Purification and characterisation of plantaricin ZJ008, a novel bacteriocin against Staphylococcus spp. from Lactobacillus plantarum ZJ008. Food chemistry, 165, 216–223. https://doi.org/10.1016/j.foodchem.2014.05.034