Abstract
1-Deoxynojirimycin (DNJ) is an efficient α-glucosidase inhibitor (α-GI) with potential applications in the prevention and treatment of diabetes. In this study, 16 Bacillus strains were screened for α-GI rate, and the strain HZ-12 with the highest α-GI rate was identified as Bacillus amyloliquefaciens through the analysis of physiological biochemical characteristics and 16S rDNA sequence. By LC-MS/Q-TOF analysis, the α-GI component produced by B. amyloliquefaciens HZ-12 was identified as DNJ. Soybean was used as the substrate for the solid-state fermentation; 870 mg/kg DNJ was produced by B. amyloliquefaciens HZ-12 after optimizing the fermentation conditions and media, which was 3.83-fold higher than the initial yield. Also, evaluations of nutraceutical enrichment in the form of anticoagulant activity, antioxidant activity, total nitrogen (TN), and total reducing sugars (TRS) of the B. amyloliquefaciens HZ-12 fermented soybeans were substantially higher than unfermented soybeans. This study provided a promising strain for high-level production of DNJ and produced nutraceutical enriched soybeans by fermentation.
Similar content being viewed by others
References
Aguilar, A. L., Escribano, J., Wentworth Jr., P., & Butters, T. D. (2014). Synthetic 1-deoxynojirimycin N-substituted peptides offer prolonged disruption to N-linked glycan processing. Chem. Med. Chem, 9, 2809–2813.
Ahuja, V., & Chou, C. H. (2016). Novel therapeutics for diabetes: uptake, usage trends, and comparative effectiveness. Current Diabetes Reports, 16, 47.
Andrew, V. R., Anne, S., Jie, F., & Inder, K. V. (2004). Synthesis of a novel photoaffinity derivative of 1-deoxynojirimycin for active site-directed labeling of glucosidase I. Glycobiology, 14, 301–310.
Asai, A., Nakagawa, K., Higuchi, O., Kimura, T., Kojima, Y., Kariya, J., Miyazawa, T., & Oikawa, S. (2011). Effect of mulberry leaf extract with enriched 1-deoxynojirimycin content on postprandial glycemic control in subjects with impaired glucose metabolism. J. Diabetes Investig, 2, 318–323.
Asano, N. (2009). Sugar-mimicking glycosidase inhibitors: bioactivity and application. Cellular and Molecular Life Sciences, 66, 1479–1492.
Baby Joseph, B. D., Hena, V., & Raj, J. (2013). Bacteriocin from Bacillus subtilis as a novel drug against diabetic foot ulcer bacterial pathogens. Asian Pac J Trop Biomed, 3, 942–946.
Bei-Zhong Han, F. M. R., & Robert Nout, M. J. (2001). A Chinese fermented soybean food. International Journal of Food Microbiology, 65, 1–10.
Butters, T. D., Dwek, R. A., & Platt, F. M. (2003). Therapeutic applications of imino sugars in lysosomal storage disorders. Current Topics in Medicinal Chemistry, 3, 561–574.
Byun, B. Y., & Mah, J. H. (2012). Occurrence of biogenic amines in Miso, Japanese traditional fermented soybean paste. Journal of Food Science, 77, T216–T223.
Chen, J., Cheng, Y.-Q., Yamaki, K., & Li, L.-T. (2007). Anti-α-glucosidase activity of Chinese traditionally fermented soybean (douchi). Food Chemistry, 103, 1091–1096.
Chen, X. H., Koumoutsi, A., Scholz, R., Eisenreich, A., Schneider, K., Heinemeyer, I., Morgenstern, B., Voss, B., Hess, W. R., Reva, O., Junge, H., Voigt, B., Jungblut, P. R., Vater, J., Sussmuth, R., Liesegang, H., Strittmatter, A., Gottschalk, G., & Borriss, R. (2007). Comparative analysis of the complete genome sequence of the plant growth-promoting bacterium Bacillus amyloliquefaciens FZB42. Nature Biotechnology, 25, 1007–1014.
Do, H. J., Chung, J. H., Hwang, J. W., Kim, O. Y., Lee, J. Y., & Shin, M. J. (2015). 1-Deoxynojirimycin isolated from Bacillus subtilis improves hepatic lipid metabolism and mitochondrial function in high-fat-fed mice. Food and Chemical Toxicology, 75, 1–7.
Eom, J. S., & Choi, H. S. (2016). Inhibition of Bacillus cereus growth and toxin production by Bacillus amyloliquefaciens RD7-7 in fermented soybean products. Journal of Microbiology and Biotechnology, 26, 44–55.
Horton, E. S. (1995). NIDDM—the devastating disease. Diabetes Research and Clinical Practice, 28, S3–S11.
Jiang, P., Mu, S., Li, H., Li, Y., Feng, C., Jin, J. M., & Tang, S. Y. (2015). Design and application of a novel high-throughput screening technique for 1-deoxynojirimycin. Scientific Reports, 5, 8563.
Juan, M. Y., & Chou, C. C. (2010). Enhancement of antioxidant activity, total phenolic and flavonoid content of black soybeans by solid state fermentation with Bacillus subtilis BCRC 14715. Food Microbiology, 27, 586–591.
Kang, K. D., Cho, Y. S., Song, J. H., Park, Y. S., Lee, J. Y., Hwang, K. Y., Rhee, S. K., Chung, J. H., Kwon, O., & Seong, S. I. (2011). Identification of the genes involved in 1-deoxynojirimycin synthesis in Bacillus subtilis MORI 3K-85. Journal of Microbiology, 49, 431–440.
Kim, J. W., Kim, S. U., Lee, H. S., Kim, I., Ahn, M. Y., & Ryu, K. S. (2003). Determination of 1-deoxynojirimycin in Morus alba L. leaves by derivatization with 9-fluorenylmethyl chloroformate followed by reversed-phase high-performance liquid chromatography. Journal of Chromatography. A, 1002, 93–99.
Kimura, T., Nakagawa, K., Kubota, H., Kojima, Y., Goto, Y., Yamagishi, K., Oita, S., Oikawa, S., & Miyazawa, T. (2007). Food-grade mulberry powder enriched with 1-deoxynojirimycin suppresses the elevation of postprandial blood glucose in humans. Journal of Agricultural and Food Chemistry, 55, 5869–5874.
Kimura, T., Nakagawa, K., Saito, Y., Yamagishi, K., Suzuki, M., Yamaki, K., Shinmoto, H., & Miyazawa, T. (2004). Simple and rapid determination of 1-deoxynojirimycin in mulberry leaves. Bio. Factors, 22, 341–345.
Ko, B. K., Ahn, H. J., van den Berg, F., Lee, C. H., & Hong, Y. S. (2009). Metabolomic insight into soy sauce through (1)H NMR spectroscopy. Journal of Agricultural and Food Chemistry, 57, 6862–6870.
Kobayashi, D., Takamura, M., Murai, H., Usui, S., Ikeda, T., Inomata, J., Takashima, S., Kato, T., Furusho, H., Takeshita, Y., Ota, T., Takamura, T., & Kaneko, S. (2010). Effect of pioglitazone on muscle sympathetic nerve activity in type 2 diabetes mellitus with alpha-glucosidase inhibitor. Autonomic Neuroscience, 158, 86–91.
Li, Y. G., Ji, D. F., Zhong, S., Lin, T. B., & Lv, Z. Q. (2015). Hypoglycemic effect of deoxynojirimycin-polysaccharide on high fat diet and streptozotocin-induced diabetic mice via regulation of hepatic glucose metabolism. Chemico-Biological Interactions, 225, 70–79.
Li, Y. G., Ji, D. F., Zhong, S., Lin, T. B., Lv, Z. Q., Hu, G. Y., & Wang, X. (2013). 1-deoxynojirimycin inhibits glucose absorption and accelerates glucose metabolism in streptozotocin-induced diabetic mice. Scientific Reports, 3, 1377.
Lijun, Y., Lite, L., Zaigui, L., Tatsumi, E., & Saito, M. (2004). Changes in isoflavone contents and composition of sufu (fermented tofu) during manufacturing. Food Chemistry, 87, 587–592.
Mo, H., Kariluoto, S., Piironen, V., Zhu, Y., Sanders, M. G., Vincken, J. P., Wolkers-Rooijackers, J., & Nout, M. J. (2013). Effect of soybean processing on content and bioaccessibility of folate, vitamin B12 and isoflavones in tofu and tempe. Food Chemistry, 141, 2418–2425.
Moy, Y. S., Lu, T. J., & Chou, C. C. (2012). Volatile components of the enzyme-ripened sufu, a Chinese traditional fermented product of soy bean. Journal of Bioscience and Bioengineering, 113, 196–201.
Onose, S., Ikeda, R., Nakagawa, K., Kimura, T., Yamagishi, K., Higuchi, O., & Miyazawa, T. (2013). Production of the alpha-glycosidase inhibitor 1-deoxynojirimycin from Bacillus species. Food Chemistry, 138, 516–523.
Parisod, H., Pakarinen, A., Kauhanen, L., Aromaa, M., Leppanen, V., Liukkonen, T. N., Smed, J., & Salantera, S. (2014). Promoting children’s health with digital games: a review of reviews. Games Health J, 3, 145–156.
Peng, Y., Huang, Q., Zhang, R. H., & Zhang, Y. Z. (2003). Purification and characterization of a fibrinolytic enzyme produced by Bacillus amyloliquefaciens DC-4 screened from douchi, a traditional Chinese soybean food. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology, 134, 45–52.
Rahati, S., Shahraki, M., Arjomand, G., & Shahraki, T. (2014). Food pattern, lifestyle and diabetes mellitus. Int. J. High Risk Behav. Addict, 3, e8725.
Scheraga, H. A. (2004). The thrombin-fibrinogen interaction. Biophysical Chemistry, 112, 117–130.
Standl, E., & Schnell, O. (2012). Alpha-glucosidase inhibitors 2012—cardiovascular considerations and trial evaluation. Diabetes & Vascular Disease Research, 9, 163–169.
Thomas, P. (2004). Isolation of Bacillus pumilus from in vitro grapes as a long-term alcohol-surviving and rhizogenesis inducing covert endophyte. Journal of Applied Microbiology, 97, 114–123.
Vichasilp, C., Nakagawa, K., Sookwong, P., Higuchi, O., Kimura, F., & Miyazawa, T. (2012). A novel gelatin crosslinking method retards release of mulberry 1-deoxynojirimycin providing a prolonged hypoglycaemic effect. Food Chemistry, 134, 1823–1830.
Wei, X., Luo, M., Xu, L., Zhang, Y., Lin, X., Kong, P., & Liu, H. (2011). Production of fibrinolytic enzyme from Bacillus amyloliquefaciens by fermentation of chickpeas, with the evaluation of the anticoagulant and antioxidant properties of chickpeas. Journal of Agricultural and Food Chemistry, 59, 3957–3963.
Wijaya-Erhardt, M., Muslimatun, S., & Erhardt, J. G. (2011). Fermented soyabean and vitamin C-rich fruit: a possibility to circumvent the further decrease of iron status among iron-deficient pregnant women in Indonesia. Public Health Nutrition, 14, 2185–2196.
Xu, B. J., Yuan, S. H., & Chang, S. K. (2007). Comparative analyses of phenolic composition, antioxidant capacity, and color of cool season legumes and other selected food legumes. Journal of Food Science, 72, S167–S177.
Yoneda, C., Tashima-Horie, K., Fukushima, S., Saito, S., Tanaka, S., Haruki, T., Ogino, J., Suzuki, Y., & Hashimoto, N. (2016). Association of morning fasting blood glucose variability with insulin antibodies and clinical factors in type 1 diabetes. Endocrine Journal, 63(7), 603–609.
Yun-Gang Jiang, C.-Y. W., Jin, C., Jia, J.-Q., Guo, X., Zhang, G.-Z., & Gui, Z.-Z. (2014). Improved 1-deoxynojirimycin (DNJ) production in mulberry leaves fermented by microorganism. Brazilian Journal of Microbiology, 45, 721–729.
Zhu, Y. P., Yamaki, K., Yoshihashi, T., Ohnishi Kameyama, M., Li, X. T., Cheng, Y. Q., Mori, Y., & Li, L. T. (2010). Purification and identification of 1-deoxynojirimycin (DNJ) in okara fermented by Bacillus subtilis B2 from Chinese traditional food (Meitaoza). Journal of Agricultural and Food Chemistry, 58, 4097–4103.
Acknowledgments
This work was supported by the National Natural Science Foundation of China (31501468), the National Science & Technology Pillar Program during the Twelfth Five-Year Plan Period (2013AA102801-52), and the Opening Project of State Key Laboratory of Agricultural Microbiology (AMLKF201403).
Authors’ Contributions
X Wei and S Chen designed the study. D Cai, M Liu, and X Li carried out the experiments for this study. D Cai, X Wei, Q Wang, C.T. Nomura, and S Chen analyzed the data and wrote the manuscript. All authors read and approved the final manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing Interests
The authors declare that they have no competing interests.
Electronic supplementary material
ESM 1
(DOC 180 kb)
Rights and permissions
About this article
Cite this article
Cai, D., Liu, M., Wei, X. et al. Use of Bacillus amyloliquefaciens HZ-12 for High-Level Production of the Blood Glucose Lowering Compound, 1-Deoxynojirimycin (DNJ), and Nutraceutical Enriched Soybeans via Fermentation. Appl Biochem Biotechnol 181, 1108–1122 (2017). https://doi.org/10.1007/s12010-016-2272-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12010-016-2272-8