Biotransformation of sesaminol triglycoside by intestinal microflora of swine supplemented with probiotic or antibiotic diet
Main Article Content
Keywords
sesame flour, sesaminol triglucoside, biotransformation, gut microbiota, probiotics
Abstract
Lignans, found throughout the plant kingdom, are complex diphenolic chemicals that act as phytoestrogens. The main lignan component in sesame flour is sesaminol triglucoside (STG). In vivo, STG is converted into antioxidant sesaminol, mammalian lignans enterodiol, and enterolactone. Thus, use of antibiotics may impact the conversion of lignans to enterolactone. The present study investigated the metabolism of STG by microorganisms in swine-fed diets supplemented with either probiotics or antibiotics. It was observed that microorganisms from swine-fed probiotics helped with hydrolyzing the glucose unit of STG and generated metabolite 2-hydroxymethyl sesaminol- tetrahydrofuran (ST-2) as compared to antibiotic diet. It was also observed that bacteria that converted sesaminol to ST-2 were oxygen-sensitive and it was hypothesized that these were anaerobes. While Lactobacillus and Bifidobacterium were more prevalent in probiotic-fed swine feces, both groups of swine had a healthy mix of helpful and detrimental bacteria. All selective investigated microorganisms (Lactobacillus, Bifidobacterium, and Clostridium perfringens) could hydrolyze the glucose unit of STG; however, lactic acid bacteria contributed least. In conclusion, the bacteria found in the feces of swine-fed probiotics had a greater ability to digest STG. It can be concluded that the biotransformation of STG could be attributable to anaerobes, but Lactobacillus and Bifidobacterium could balance intestinal flora.
References
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Landete, J.M., 2012. Plant and mammalian lignans: a review of source, intake, metabolism, intestinal bacterial and health. Food Research International 46: 410−424. 10.1016/j.foodres.2011.12.023
Ley, R.E., Lozupone, C.A., Hamady, C.A., Knight, R. and Gordon, J.I., 2008. Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Reviews Microbiology 6: 776−788. 10.1038/nrmicro1978
Liao, C.D., Hung, W.L., Lu, W.C., Jan, K.C., Shih, D.Y.C., Yeh, A.I., Ho, C.T. and Hwang, L.S., 2010. Differential tissue distribution of sesaminol triglucoside and its metabolites in rats fed with lignan glycosides from sesame meal with or without nano/submicrosizing. Journal of Agricultural and Food Chemistry 58: 563−569. 10.1021/jf9028046
Meléndez-Martínez, A.J., Pérez-Gálvez, A., Roca, M., Estévez-Santiago, R., OlmedillaAlonso, B., Mercadante, A.Z., et al., 2017. Biodisponibilidad de carotenoides, factores que la determinan y métodos de estimación. In: Meléndez-Martínez, A.J. (ed.) Carotenoides en agroalimentación Y salud. CYTED: Madrid, Spain; pp. 574–608.
Mitsiopoulou, C., Karaiskou, C., Simoni, M., Righi, F., Pappas, A.C., Sotirakoglou, K. and Tsiplakou, E., 2021. Influence of dietary sesame meal, vitamin E and selenium supplementation on milk production, composition, and fatty acid profile in dairy goats. Livestock Science 244: 104336. 10.1016/j.livsci.2020.104336
Mokhtarian, M., Tavakolipour, H., Bagheri, F., Oliveira, C.A.F., Corassin, C.H. and Khaneghah, A.M., 2020. Aflatoxin B1 in the Iranian pistachio nut and decontamination methods: a systematic review. Quality Assurance and Safety of Crops & Foods 12(4): 15–25. 10.15586/qas.v12i4.784
Munoa, F.J. and Pares, R., 1988. Selective medium for isolation and enumeration of Bifidobacterium spp. Applied and Environmental Microbiology 54: 1715–1718. 10.1128/aem.54.7.1715-1718.1988
Ramirez, J., Guarner, F., Bustos Fernandez, L., Maruy, A., Sdepanian, V.L., Cohen, H., 2020. Antibiotics as major disruptors of gut microbiota. Frontiers in Cellular and Infection Microbiology 24(10): 572912. 10.3389/fcimb.2020.572912
Rietjens, I.M., Louisse, J. and Beekmann, K., 2017. The potential health effects of dietary phytoestrogens. British Journal of Pharmacology 174: 1263–1280. 10.1111/bph.13622
Rodriguez-Concepcion, M., Avalos, J., Bonet, M.L., Boronat, A., Gomez-Gomez, L., Hornero-Mendez, D., 2018. A global perspective on carotenoids: metabolism, biotechnology, and benefits for nutrition and health. Progress in Lipid Research 70: 62–93. 10.1016/j.plipres.2018.04.004
Suja, K.P., Jayalekshmy, A., Arumughan, C., 2005. Antioxidant activity of sesame cake extract. Food Chemistry 91: 213−219. 10.1016/j.foodchem.2003.09.001
Tufail, T., Riaz, M., Arshad, M.U., Gilani, S.A., Ul Ain, H.B., Khursheed, T., Islam, Z., Imran, M., Bashir, S., Zia Shahid, M., Kazmi, S.M.U., Saqib, A., 2020. Functional and nutraceutical scenario of flaxseed and sesame. International Journal of Biological Sciences 17: 173–190.
Wang, J.L., Zhao, F., Cairang, Z.M., Li, X.Y., Kong, J., Zeng, S.Y., et al., 2021. Correlation between the bacterial community and flavour of fermented fish. Quality Assurance and Safety of Crops & Foods 13(3): 82–91. 10.15586/qas.v13i3.908
Woting, A., Clavel, T., Loh, G. and Blaut, M., 2010. Bacterial transformation of dietary lignans in gnotobiotic rats. FEMS Microbiology Ecology 72: 507–514. 10.1111/j.1574-6941.2010.00863.x
Zhu, X., Zhang, X., Sun, Y., Su, D., Sun, Y., Hu, B. and Zeng, X., 2013. Purification and fermentation in vitro of sesaminol triglucoside from sesame cake by human intestinal microbiota. Journal of Agricultural and Food Chemistry 61: 1868–1877. 10.1021/jf304643k
Andargie, M., Vinas, M., Rathgeb, A., Möller, E. and Karlovsky, P., 2021. Lignans of sesame (Sesamum indicum L.): a comprehensive review. Molecules 26(4): 883. 10.3390/molecules26040883
Chhillar, H., Chopra, P. and Ashfaq, M.A., 2021. Lignans from linseed (Linum usitatissimum L.) and its allied species: retrospect, introspect and prospect. Critical Reviews in Food Science and Nutrition 61(16): 2719–2741. 10.1080/10408398.2020.1784840
Christensen, D.N., Bach Knudsen, K.E., Wolstrup, J. and Jensen, B.B., 1999. Integration of ileum cannulated pigs and in vitro fermentation to quantify the effect of diet composition on the amount of short-chain fatty acids available from fermentation in the large intestine. Journal of the Science of Food and Agriculture 79: 755–762. 10.1002/(SICI)1097-0010(199904)79:5<755::AID-JSFA248>3.0.CO;2-2
Clavel, T., Borrmann, D., Braune, A., Doré, J. and Blauta, M., 2006. Occurrence and activity of human intestinal bacteria involved in the conversion of dietary lignans. Anaerobe 12: 140−147. 10.1016/j.anaerobe.2005.11.002
Gavahian, M., Khaneghah, A.M., Lorenzo, J.M., Munekata, P.E., Garcia-Mantrana, I., Collado, M.C. and Barba, F.J., 2019. Health benefits of olive oil and its components: impacts on gut micro-biota antioxidant activities, and prevention of noncommunicable diseases. Trends in Food Science Technology 88: 220–227. 10.1016/j.tifs.2019.03.008
Hameed, A.S.S., Rawat, P.S., Meng, X. and Liu, W., 2020. Biotransformation of dietary phytoestrogens by gut microbes: a review on bi-directional interaction between phytoestrogen metabolism and gut microbiota. Biotechnology Advances 43: 107576. 10.1016/j.biotechadv.2020.107576
Hano, C.F., Dinkova-Kostova, A.T., Davin, L.B., Cort, J.R. and Lewis, N.G., 2021. Lignans: insights into their biosynthesis, metabolic engineering, analytical methods and health benefits. Frontiers in Plant Science 11: 2142. 10.3389/978-2-88966-491-7; 10.3389/fpls.2020.630327
Harmon, S.M., Kautter, D.A. and Peeler, J.T., 1971. Improved medium for enumeration of Clostridium perfringens. Journal of Applied Microbiology 22: 688–692. 10.1128/am.22.4.688-692.1971
Hung W.L., Liao C.D., Lu W.C., Ho C.T., Hwang L.S., 2016. Lignan glycosides from sesame meal exhibit higher oral bioavail-ability and antioxidant activity in rat after nano/submicro-sizing. Journal of Functional Foods 23: 511–522. 10.1016/j.jff.2016.03.008
Ianiro G., Tilg H. and Gasbarrini A., 2016. Antibiotics as deep modulators of gut microbiota: between good and evil. Gut 65(11): 1906–1915. 10.1136/gutjnl-2016-312297
Jan, K.C., Hwang, L.S. and Ho, C.T., 2009a. Biotransformation of sesaminol triglucoside to mammalian lignans by intestinal microbiota. Journal of Agricultural and Food Chemistry 57: 6101−6106. 10.1021/jf901215j
Jan, K.C., Hwang, L.S. and Ho, C.T., 2009b. Tissue distribution and elimination of sesaminol triglucoside and its metabolites in rat. Molecular Nutrition & Food Research 53: 815−825. 10.1002/mnfr.200800380
Jan, K.C., Ku, K.L., Chu, Y.H., Hwang, L.S. and Ho, C.T., 2010. Tissue distribution and elimination of estrogenic and anti-inflammatory catechol metabolites from sesaminol trigluco-side in rats. Journal of Agricultural and Food Chemistry 58: 7693−7700. 10.1021/jf1009632
Jan, K.C., Ku, K.L., Chu, Y.H., Hwang, L.S. and Ho, C.T., 2011. Intestinal distribution and excretion of sesaminol and its tetrahydrofuranoid metabolites in rats. Journal of Agricultural and Food Chemistry 59: 3078−3086. 10.1021/jf105012v
Jensen, M.T., Cox, R.P. and Jensen, B.B., 1995. Microbial production of skatole in the hind gut of pigs fed different diets and its relation to skatole deposition in backfat. Journal of Animal Science, 61: 293–304. 10.1017/S1357729800013837
Kamal-Eldin, A., Moazzami, A. and Washi, S., 2011. Sesame seed lignans: potent physiological modulators and possible ingredients in functional foods & nutraceuticals. Recent Patents on Food, Nutrition & Agriculture 3: 17−29. 10.2174/2212798411103010017
Landete, J.M., 2012. Plant and mammalian lignans: a review of source, intake, metabolism, intestinal bacterial and health. Food Research International 46: 410−424. 10.1016/j.foodres.2011.12.023
Ley, R.E., Lozupone, C.A., Hamady, C.A., Knight, R. and Gordon, J.I., 2008. Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Reviews Microbiology 6: 776−788. 10.1038/nrmicro1978
Liao, C.D., Hung, W.L., Lu, W.C., Jan, K.C., Shih, D.Y.C., Yeh, A.I., Ho, C.T. and Hwang, L.S., 2010. Differential tissue distribution of sesaminol triglucoside and its metabolites in rats fed with lignan glycosides from sesame meal with or without nano/submicrosizing. Journal of Agricultural and Food Chemistry 58: 563−569. 10.1021/jf9028046
Meléndez-Martínez, A.J., Pérez-Gálvez, A., Roca, M., Estévez-Santiago, R., OlmedillaAlonso, B., Mercadante, A.Z., et al., 2017. Biodisponibilidad de carotenoides, factores que la determinan y métodos de estimación. In: Meléndez-Martínez, A.J. (ed.) Carotenoides en agroalimentación Y salud. CYTED: Madrid, Spain; pp. 574–608.
Mitsiopoulou, C., Karaiskou, C., Simoni, M., Righi, F., Pappas, A.C., Sotirakoglou, K. and Tsiplakou, E., 2021. Influence of dietary sesame meal, vitamin E and selenium supplementation on milk production, composition, and fatty acid profile in dairy goats. Livestock Science 244: 104336. 10.1016/j.livsci.2020.104336
Mokhtarian, M., Tavakolipour, H., Bagheri, F., Oliveira, C.A.F., Corassin, C.H. and Khaneghah, A.M., 2020. Aflatoxin B1 in the Iranian pistachio nut and decontamination methods: a systematic review. Quality Assurance and Safety of Crops & Foods 12(4): 15–25. 10.15586/qas.v12i4.784
Munoa, F.J. and Pares, R., 1988. Selective medium for isolation and enumeration of Bifidobacterium spp. Applied and Environmental Microbiology 54: 1715–1718. 10.1128/aem.54.7.1715-1718.1988
Ramirez, J., Guarner, F., Bustos Fernandez, L., Maruy, A., Sdepanian, V.L., Cohen, H., 2020. Antibiotics as major disruptors of gut microbiota. Frontiers in Cellular and Infection Microbiology 24(10): 572912. 10.3389/fcimb.2020.572912
Rietjens, I.M., Louisse, J. and Beekmann, K., 2017. The potential health effects of dietary phytoestrogens. British Journal of Pharmacology 174: 1263–1280. 10.1111/bph.13622
Rodriguez-Concepcion, M., Avalos, J., Bonet, M.L., Boronat, A., Gomez-Gomez, L., Hornero-Mendez, D., 2018. A global perspective on carotenoids: metabolism, biotechnology, and benefits for nutrition and health. Progress in Lipid Research 70: 62–93. 10.1016/j.plipres.2018.04.004
Suja, K.P., Jayalekshmy, A., Arumughan, C., 2005. Antioxidant activity of sesame cake extract. Food Chemistry 91: 213−219. 10.1016/j.foodchem.2003.09.001
Tufail, T., Riaz, M., Arshad, M.U., Gilani, S.A., Ul Ain, H.B., Khursheed, T., Islam, Z., Imran, M., Bashir, S., Zia Shahid, M., Kazmi, S.M.U., Saqib, A., 2020. Functional and nutraceutical scenario of flaxseed and sesame. International Journal of Biological Sciences 17: 173–190.
Wang, J.L., Zhao, F., Cairang, Z.M., Li, X.Y., Kong, J., Zeng, S.Y., et al., 2021. Correlation between the bacterial community and flavour of fermented fish. Quality Assurance and Safety of Crops & Foods 13(3): 82–91. 10.15586/qas.v13i3.908
Woting, A., Clavel, T., Loh, G. and Blaut, M., 2010. Bacterial transformation of dietary lignans in gnotobiotic rats. FEMS Microbiology Ecology 72: 507–514. 10.1111/j.1574-6941.2010.00863.x
Zhu, X., Zhang, X., Sun, Y., Su, D., Sun, Y., Hu, B. and Zeng, X., 2013. Purification and fermentation in vitro of sesaminol triglucoside from sesame cake by human intestinal microbiota. Journal of Agricultural and Food Chemistry 61: 1868–1877. 10.1021/jf304643k
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