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Primary and Secondary Metabolites Variation of Soybean Contaminated with Aspergillus Sojae

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Primary and Secondary Metabolites Variation of Soybean Contaminated with Aspergillus Sojae Food Research International 54 (2013) 487–494 Contents lists available at SciVerse ScienceDirect Food Research International journal homepage: www.elsevier.com/locate/foodres Primary and secondary metabolites variation of soybean contaminated with Aspergillus sojae K.M. Maria John a,EunSungJunga,SarahLeea, Jong-Sang Kim b, Choong Hwan Lee a,⁎ a Department of Bioscience and Biotechnology, Konkuk University, Seoul 143-701, Republic of Korea b School of Food Science and Biotechnology, Kyungpook National University, Daegu 702-701, Republic of Korea article info abstract Article history: Time-dependent primary and secondary metabolite changes of soybean contaminated with Aspergillus sojae and Received 23 April 2013 their associations were discussed. Partial least squares discriminant analysis showed that the patterns of fungus Accepted 15 July 2013 infected soybean were clearly distinguished from untreated samples based on its time intervals. A. sojae depends Available online 22 July 2013 on soybean for its carbon source resulting gradual decrease in the glucose, fructose and myo-inositol levels. The stimulation in L-phenylalanine by A. sojae increases the accumulation of naringenin from days 1 to 6, leading Keywords: to the changes in genistein pool. Even though the level of glucosides like daidzin, genistin and glycitin decreased Aspergillus sojae fl Gas chromatography–time of flight–mass during treatment, other iso avones and coumestan levels enhanced. Due to the increase in glycinol, the resulting spectrometry (GC-TOF-MS) phytoalexins such as glyceollin I and glyceollin II augmented by fungal treatment. The changes in secondary Isoflavones metabolites reflects in total phenolic content and because of the increase in glyceollin I, II and glyceofuran re- Phytoalexins flect their radical scavenging capacity; A. sojae-mediated soybean registered a periodic increase in the radical Ultra performance liquid chromatography scavenging activity. fl quadrupole time of ight mass spectrometry © 2013 Elsevier Ltd. All rights reserved. (UPLC-Q-TOF-MS) 1. Introduction potential (Jeon et al., 2012; Kim, Suh, Kim, Park, et al., 2010), as well as its estrogenic activity (Burow et al., 2001; Kim, Suh, Kim, Kang, From ancient times, food has been metabolically changed by pro- et al., 2010). Moreover, antioxidant capacity of germinating soybean in- cessing via microbial fermentation. Soybean is well known for its high duced by A. oryzae was reported by Jeon et al., 2012. content of isoflavones, which show numerous health benefits, such as Simons, Vincken, Bohinm, et al. (2011) screened for the presence antioxidant potential (Kim, Song, Kwon, Kim, & Heo, 2008; Ng et al., of prenylated isoflavonoids with a liquid chromatography/mass 2011) and anti-diabetic activity (Kwon, Daily, Kim, & Park, 2010; Park, spectrometry (LC/MS)-based screening method, in which they used Kim, Kim, Kim, & Kim, 2012). Fermented soy food products are promi- R. microspores-mediated metabolic changes on germinated soy seed. nent in Asian countries, like China, Japan and Korea. Numerous research Boue, Carter, Ehrlich, and Cleveland (2000) studied the induction and findings illustrate that metabolic changes in soy-based food is enhanced accumulation of phytoalexins in soybean cotyledon tissue, using 4 spe- by microbial fermentation. Cheonggukjang (Baek et al., 2010; Kim et al., cies of Aspergillus: A. sojae, A. oryzae, A. niger and A. flavus, but reported 2011; Park et al., 2010), Douche (Fan, Zhang, Chang, Saito, & Li, 2009) only glyceollin I, glyceollin II and glyceollin III and coumestrol changes and Meju (Kang et al., 2011; Lee, Kim, et al., 2012) are some of the during treatment. Coumestan and pterocarpan changes varied based well-known traditional Korean fermented soy food studied with regard on the fungus, indicating that the levels of metabolites will change to metabolic changes and antioxidant activities (Kim et al., 2008). based on fungal type. The condition of the soybean used for fungal treat- Recently, fungus-mediated changes in secondary metabolite content ment is another point of concern. Previous studies report the use of and the correlation of these changes with antioxidant activities were intact seed (Kim, Suh, Kim, Park, et al., 2010), germinating seeds (Jeon documented in soybean. Aspergillus oryzae (Jeon, Seo, Shin, & Lee, et al., 2012; Simons, Vincken, Bohinm, et al., 2011; Simons, Vincken, 2012), Aspergillus sojae (Kim, Suh, Kim, Kang, et al., 2010; Kim, Suh, Roidos, et al., 2011) and half-broken seeds (Boue et al., 2000) for fungal Kim, Park, et al., 2010; Ojokoh, Shi, Hujia, & Liang, 2012)andRhizopus treatment. In all these studies, only secondary metabolites changes, microspores (Simons, Vincken, Bohinm, et al., 2011; Simons, Vincken, particularly those relating to glyceollin, have been reported. Simons, Roidos, et al., 2011) were used to infect soybean seeds to produce met- Vincken, Roidos, et al. (2011) reported changes in 30 secondary compo- abolic changes. Glyceollin, a phytoalexin present in soybean, has been nents and 1 primary metabolite, viz., phenylalanine, influenced by extensively studied with regard to changes in its level and antioxidant R. microspores. Even though the primary metabolite changes during fer- mentation of soy-based food has been reported (Kim et al., 2011), the ⁎ Corresponding author. Tel.: +82 2 2049 6177; fax: +82 2 455 4291. changes induced in soybean seeds by fungal treatment have not yet E-mail address: [email protected] (C.H. Lee). been compared. Such a study will help to understand the mechanism 0963-9969/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.foodres.2013.07.045 488 K.M.M. John et al. / Food Research International 54 (2013) 487–494 underlying metabolite changes during fungal treatment. Therefore, 2.5. Sample preparation for secondary metabolite analysis this study aimed to identify the variation in primary and secondary metabolites of soybean contaminated with A. sojae.Theroleofprimary Soybean samples (0.2 g) were extracted with 1.5 mL of 80% (v/v) metabolites and their associations with secondary metabolite changes methanol, followed by vigorous shaking for a period of 3 min in a are also discussed. mixer mill. After 2 min of sonication, the extracts were centrifuged at 10,000 rpm for 5 min. Supernatants were collected and dried under speed vacuum. The dried extracts were again dissolved with 500 μLof 2. Materials and methods methanol, followed by filtering through a sterile syringe filter (PTFE) with a 0.45-μm pore size, prior to analysis. 2.1. Chemicals and reagents 2.6. Ultra-performance liquid chromatography–quadrupole time of HPLC-grade water, methanol and acetonitrile were purchased from flight–mass spectrometry (UPLC-Q-TOF-MS) analysis Burdick and Jackson (Muskegon, MI, USA). All standards and other ′ chemicals, like 2,2 -azinobis (3-ethylbenzothiazoline-6-sulfonic acid) Secondary metabolite extracts of soybean samples were analyzed diammonium salt (ABTS) and 1,1-diphenyl-2-picrylhydrazyl (DPPH), using a Waters Micromass Q-TOF Premier UPLC-Q-TOF-MS system were obtained from Sigma Aldrich (St. Louis, MO, USA). with UPLC Acquity System (Waters, Milford, MA, USA). Analysis was performed employing an Acquity UPLC BEH C18 column (100 × 2.1 mm, Waters) with a particle size of 1.7 μm. The mobile 2.2. Sample preparation phase consisted of water (A) and acetonitrile (B) with 0.1% formic acid (v/v). Five microliters of the sample was injected, and the flow Soybean (Aga No. 3) showing exceedingly high levels of isoflavones rate was maintained at 0.3 mL/min. ESI was performed in the negative were obtained from Kyungpook National University Soy venture Co., (−) and positive (+) ion mode within a range of 100–1,000 m/z. Ltd. (Daegu, South Korea) and were subjected to treat with A. sojae to The operating parameters were as follows: ion source temperature, evaluate metabolic changes during treatment. A. sojae cultures were 200 °C; cone gas flow, 50 L/h; desolvation gas flow, 600 L/h; capillary grown at 25 °C in the dark on potato dextrose agar (PDA) media for voltage, 2.8 kV; and cone voltage, up to 35 V. a period of 5 days. Inocula were prepared by harvesting fungi after 5 days of incubation. 2.7. Data processing Dried soybeans were surface sterilized for 3 min with 70% ethanol prior to presoaked in sterile deionized water for 4–5 h. Soybean seeds GC-TOF-MS raw data files were converted to computable document were crumbled using a food homogenizer (Hanil, Bucheon, S. Korea) format (*.cdf) by the inbuilt data processing software of the Agilent before fungal treatment under controlled treatment chamber. A. sojae GC system programs. Raw UPLC-Q-TOF data sets were converted to a spore suspension (10 μL) was evenly spread across the soybeans, NetCDF file (*.cdf) format using MassLynx software (version 4.1, Waters followed by placing in a chamber at 26 °C in the dark for 7 days. After Corp). After obtaining the CDF format, the files were subjected to pre- sterilization, the samples were stored at −20 °C; in the meantime, sam- processing, peak extraction, retention time correction and alignment ples were collected daily over the period of 7 days and were powdered using metAlign software package (http://www.metalign.nl). After and freeze-dried. The whole experiment for sample preparation was analysis, the resulting peak list was obtained as a .txt file, which was repeated three times and were analyzed for primary and secondary me- later exported to Microsoft Excel (Microsoft, Redmond, WA, USA). The tabolite content. Excel file contained the corrected peak retention time, peak area and corresponding mass (m/z) data matrix for further analysis. 2.3. Sample preparation for primary metabolite analysis 2.8. Multivariate analysis Lyophilized soybean samples (100 mg) along with the control (0 day, uninfected) were extracted with 1 mL of methanol:water:chloroform Primary and secondary metabolites underwent multivariate sta- fl (2.5:1:1 v:v:v) containing norvaline as internal standard.
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