Abstract
The aim of the study was to investigate the dynamic changes of mycobiota community, and the resultant effects on the antioxidant properties during the Chinese bayberry Jiaosu fermentation. The structure and composition of mycobiota during the Chinese bayberry Jiaosu fermentation were significantly changed (p < 0.001) and clearly clustered into two distinct phases (Phase 1: Day 5–20; Phase 2: Day 30–60, p < 0.001). From Phase 1 to Phase 2, the dominant fungi gradually changed from Saccharomycetales fam Incertae sedis to Saccharomyces cerevisiae. The antioxidative properties (total polyphenols, 1,1-diphenyl-2-picrylhydrazyl [DPPH], superoxide and 2,2′-azino-bis-(3-ethylbenzthiazoline-6-sulphonate) [ABTS] radical scavenging) of Chinese bayberry Jiaosu were significantly increased by 250.4, 73.9, 25.3 and 40.0% respectively (p < 0.001). Co-occurrence network analysis revealed that Saccharomyces cerevisiae contributed to the increase of antioxidative properties in the Chinese bayberry Jiaosu fermentation. Our research indicates that fermentation into Chinese bayberry Jiaosu is an effective and new method for high-valued utilization of Chinese bayberry.
Funding source: Zhejiang Provincial Key Research and Development Project
Award Identifier / Grant number: 2017C02009
Funding source: Zhejiang Provincial Education Department General Project
Award Identifier / Grant number: Y201839416
Funding source: Zhejiang Provincial Natural Science Foundation of China
Award Identifier / Grant number: LQ19C200005
Funding source: Shaoxing Science and Technology Project
Award Identifier / Grant number: 2018C20009
Author contributions: Sheng Fang: Investigation, Formal analysis, Writing – original draft, Writing – review & editing. Zhening Jin: Investigation, Formal analysis, Conceptualization, Methodology. Yisong Xu: Investigation, Data curation, Methodology, Writing – review & editing. Ruyi Sha: Supervision, Writing – review & editing; Jianwei Mao: Supervision, Writing – review & editing; Zengliang Jiang: Supervision, Project administration, Writing – review & editing.
Research funding: This study was funded by Zhejiang Provincial Key Research and Development Project (Grant No. 2017C02009), Shaoxing Science and Technology Project (Grant No. 2018C20009), Zhejiang Provincial Natural Science Foundation of China (Grant No. LQ19C200005) and Zhejiang Provincial Education Department General Project (Grant No. Y201839416).
Conflict of interest statement: The authors declare no conflict of interest.
References
1. Association CBFIA. Guideline for classification of Jiaosu products (T/CBFIA 08001–2016). Beijing, China: China Biotech Fermentation Industry Association; 2016.Search in Google Scholar
2. Feng, YJ, Zhang, M, Mujumdar, AS, Gao, ZX. Recent research process of fermented plant extract: a review. Trends Food Sci Technol 2017;65:40–8. https://doi.org/10.1016/j.tifs.2017.04.006.Search in Google Scholar
3. Dai, J, Sha, R, Wang, ZZ, Cui, YL, Fang, S, Mao, JW. Edible plant Jiaosu: manufacturing, bioactive compounds, potential health benefits, and safety aspects. J Sci Food Agric 2020;100:5313–23. https://doi.org/10.1002/jsfa.10518.Search in Google Scholar
4. Pena-Bautista, C, Baquero, M, Vento, M, Chafer-Pericas, C. Free radicals in Alzheimer’s disease: lipid peroxidation biomarkers. Clin Chim Acta 2019;491:85–90. https://doi.org/10.1016/j.cca.2019.01.021.Search in Google Scholar
5. Sas, K, Szabo, E, Vecsei, L. Mitochondria, oxidative stress and the kynurenine system, with a focus on ageing and neuroprotection. Molecules 2018;23. https://doi.org/10.3390/molecules23010191.Search in Google Scholar
6. Singh, R, Devi, S, Gollen, R. Role of free radical in atherosclerosis, diabetes and dyslipidaemia: larger-than-life. Diabetes Metab Res Rev 2015;31:113–26. https://doi.org/10.1002/dmrr.2558.Search in Google Scholar
7. Hifney, AF, Fawzy, MA, Abdel-Gawad, KM, Gomaa, M. Upgrading the antioxidant properties of fucoidan and alginate from Cystoseira trinodis by fungal fermentation or enzymatic pretreatment of the seaweed biomass. Food Chem 2018;269:387–95. https://doi.org/10.1016/j.foodchem.2018.07.026.Search in Google Scholar
8. Alves, JA, Lima, LCD, Dias, DR, Nunes, CA, Schwan, RF. Effects of spontaneous and inoculated fermentation on the volatile profile of lychee (Litchi chinensis Sonn) fermented beverages. Int J Food Sci Technol 2010;45:2358–65. https://doi.org/10.1111/j.1365-2621.2010.02409.x.Search in Google Scholar
9. Ma, D, He, QW, Ding, J, Wang, HY, Zhang, HP, Kwok, LY. Bacterial microbiota composition of fermented fruit and vegetable juices (jiaosu) analyzed by single-molecule, real-time (SMRT) sequencing. CyTA – J Food 2018;16:950–6. https://doi.org/10.1080/19476337.2018.1512531.Search in Google Scholar
10. Ren, HY, Yu, HY, Zhang, SW, Liang, SM, Zheng, XL, Zhang, SJ, et al.. Genome sequencing provides insights into the evolution and antioxidant activity of Chinese bayberry. BMC Genom 2019;20. https://doi.org/10.1186/s12864-019-5818-7.Search in Google Scholar
11. Wang, KT, Cao, SF, Jin, P, Rui, HJ, Zheng, YH. Effect of hot air treatment on postharvest mould decay in Chinese bayberry fruit and the possible mechanisms. Int J Food Microbiol 2010;141:11–6. https://doi.org/10.1016/j.ijfoodmicro.2010.05.004.Search in Google Scholar
12. Tian, J, Cao, Y, Chen, S, Fang, Z, Chen, J, Liu, D, et al.. Juices processing characteristics of Chinese bayberry from different cultivars. Food Sci Nutr 2019;7:404–11. https://doi.org/10.1002/fsn3.778.Search in Google Scholar
13. Zhang, XN, Huang, HZ, Zhang, QL, Fan, FJ, Xu, CJ, Sun, CD, et al.. Phytochemical characterization of Chinese bayberry (Myrica rubra Sieb. et Zucc.) of 17 cultivars and their antioxidant properties. Int J Mol Sci 2015;16:12467–81. https://doi.org/10.3390/ijms160612467.Search in Google Scholar
14. Jiang, ZL, Mao, JW, Huang, J, Wu, YF, Cai, CG. Changes in antioxidant activity of grape-ferment in vitro during natural fermentation process. J Chin Inst Food Sci Technol 2014;14:29–34.Search in Google Scholar
15. Edgar, RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 2013;10:996–8. https://doi.org/10.1038/nmeth.2604.Search in Google Scholar
16. Prior, RL, Wu, X, Schaich, K. Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 2005;53:4290–302. https://doi.org/10.1021/jf0502698.Search in Google Scholar
17. Yen, GC, Chen, HY. Antioxidant activity of various tea extracts in relation to their antimutagenicity. J Agric Food Chem 1994;43:27–32.10.1021/jf00049a007Search in Google Scholar
18. Blois, MS. Antioxidant determination by use of a stable free radical. Nature 1958;181:1199–200. https://doi.org/10.1038/1811199a0.Search in Google Scholar
19. Re, R, Pellegrini, N, Proteggente, A, Pannala, A, Yang, M, Rice-Evans, C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 1999;26:1231–7. https://doi.org/10.1016/s0891-5849(98)00315-3.Search in Google Scholar
20. Prado, FC, Lindner, JD, Inaba, J, Thomaz-Soccol, V, Bray, SK, Soccol, CR. Development and evaluation of a fermented coconut water beverage with potential health benefits. J Funct Foods 2015;12:489–97.10.1016/j.jff.2014.12.020Search in Google Scholar
21. Arroyo-Lopez, FN, Medina, E, Ruiz-Bellido, MA, Romero-Gil, V, Montes-Borrego, M, Landa, BB. Enhancement of the knowledge on fungal communities in directly brined Alorena de Malaga green olive fermentations by metabarcoding analysis. PloS One 2016;11. https://doi.org/10.1371/journal.pone.0163135.Search in Google Scholar
22. Coton, M, Pawtowski, A, Taminiau, B, Burgaud, G, Deniel, F, Coulloumme-Labarthe, L, et al.. Unraveling microbial ecology of industrial-scale Kombucha fermentations by metabarcoding and culture-based methods. FEMS Microbiol Ecol 2017;93. https://doi.org/10.1093/femsec/fix048.Search in Google Scholar
23. Rai, AK, Appaiah, KAA. Application of native yeast from Garcinia (Garcinia xanthochumus) for the preparation of fermented beverage: changes in biochemical and antioxidant properties. Food Biosci 2014;5:101–7. https://doi.org/10.1016/j.fbio.2013.11.008.Search in Google Scholar
24. Duangjitcharoen, Y, Kantachote, D, Ongsakul, M, Poosaran, N, Chaiyasut, C. Potential use of probiotic Lactobacillus plantarum SS2 isolated from a fermented plant beverage: safety assessment and persistence in the murine gastrointestinal tract. World J Microbiol Biotechnol 2009;25:315–21. https://doi.org/10.1007/s11274-008-9894-0.Search in Google Scholar
25. Botes, A, Todorov, SD, von Mollendorff, JW, Botha, A, Dicks, LMT. Identification of lactic acid bacteria and yeast from boza. Process Biochem 2007;42:267–70. https://doi.org/10.1016/j.procbio.2006.07.015.Search in Google Scholar
26. Kumar, M, Ghosh, M, Ganguli, A. Mitogenic response and probiotic characteristics of lactic acid bacteria isolated from indigenously pickled vegetables and fermented beverages. World J Microbiol Biotechnol 2012;28:703–11. https://doi.org/10.1007/s11274-011-0866-4.Search in Google Scholar
27. Aloulou, A, Hamden, K, Elloumi, D, Ali, MB, Hargafi, K, Jaouadi, B, et al.. Hypoglycemic and antilipidemic properties of kombucha tea in alloxan-induced diabetic rats. BMC Compl Alternative Med 2012;12. https://doi.org/10.1186/1472-6882-12-63.Search in Google Scholar
28. Marsh, AJ, O’Sullivan, O, Hill, C, Ross, RP, Cotter, PD. Sequence-based analysis of the bacterial and fungal compositions of multiple kombucha (tea fungus) samples. Food Microbiol 2014;38:171–8. https://doi.org/10.1016/j.fm.2013.09.003.Search in Google Scholar
29. Teoh, AL, Heard, G, Cox, J. Yeast ecology of Kombucha fermentation. Int J Food Microbiol 2004;95:119–26. https://doi.org/10.1016/j.ijfoodmicro.2003.12.020.Search in Google Scholar
30. Ponomarova, O, Gabrielli, N, Sevin, DC, Mulleder, M, Zimgibl, K, Bulyha, K, et al.. Yeast creates a niche for symbiotic lactic acid bacteria through nitrogen overflow. Cell Syst 2017;5:345–+. https://doi.org/10.1016/j.cels.2017.09.002.Search in Google Scholar
31. Batifoulier, F, Verny, MA, Chanliaud, E, Remesy, C, Demigne, C. Effect of different breadmaking methods on thiamine, riboflavin and pyridoxine contents of wheat bread. J Cereal Sci 2005;42:101–8. https://doi.org/10.1016/j.jcs.2005.03.003.Search in Google Scholar
32. Gobbetti, M, Rizzello, CG, Di Cagno, R, De Angelis, M. How the sourdough may affect the functional features of leavened baked goods. Food Microbiol 2014;37:30–40. https://doi.org/10.1016/j.fm.2013.04.012.Search in Google Scholar
33. Burgos-Edwards, A, Jimenez-Aspee, F, Theoduloz, C, Schmeda-Hirschmann, G. Colonic fermentation of polyphenols from Chilean currants (Ribes spp.) and its effect on antioxidant capacity and metabolic syndrome-associated enzymes. Food Chem 2018;258:144–55. https://doi.org/10.1016/j.foodchem.2018.03.053.Search in Google Scholar
34. Kim, DH, Kim, MJ, Kim, DW, Kim, GY, Kim, JK, Gebru, YA, et al.. Changes of phytochemical components (urushiols, polyphenols, gallotannins) and antioxidant capacity during fomitella fraxinea-mediated fermentation of toxicodendron vernicifluum bark. Molecules 2019;24. https://doi.org/10.3390/molecules24040683.Search in Google Scholar
35. Albertini, B, Schoubben, A, Guarnaccia, D, Pinelli, F, Della Vecchia, M, Ricci, M, et al.. Effect of fermentation and drying on cocoa polyphenols. J Agric Food Chem 2015;63:9948–53. https://doi.org/10.1021/acs.jafc.5b01062.Search in Google Scholar
36. Du, X, Myracle, AD. Fermentation alters the bioaccessible phenolic compounds and increases the alpha-glucosidase inhibitory effects of aronia juice in a dairy matrix following in vitro digestion. Food Funct 2018;9:2998–3007. https://doi.org/10.1039/c8fo00250a.Search in Google Scholar
37. Toktas, B, Bildik, F, Ozcelik, B. Effect of fermentation on anthocyanin stability and in vitro bioaccessibility during shalgam (algam) beverage production. J Sci Food Agric 2018;98:3066–75.10.1002/jsfa.8806Search in Google Scholar
38. Chen, T, Piao, M, Ehsanur Rahman, SM, Zhang, L, Deng, Y. Influence of fermentation on antioxidant and hypolipidemic properties of maifanite mineral water-cultured common buckwheat sprouts. Food Chem 2020;321:126741. https://doi.org/10.1016/j.foodchem.2020.126741.Search in Google Scholar
39. Grieco, F, Carluccio, MA, Giovinazzo, G. Autochthonous Saccharomyces cerevisiae starter cultures enhance polyphenols content, antioxidant activity, and anti-inflammatory response of apulian red wines. Foods 2019;8:453. https://doi.org/10.3390/foods8100453.Search in Google Scholar
40. Patel, V, Tripathi, AD, Adhikari, KS, Srivastava, A. Screening of physicochemical and functional attributes of fermented beverage (wine) produced from local mango (Mangifera indica) varieties of Uttar Pradesh using novel saccharomyces strain. J Food Sci Technol 2020;1:1–10. https://doi.org/10.1007/s13197-020-04731-9.Search in Google Scholar
41. Ju, HK, Cho, EJ, Jang, MH, Lee, YY, Hong, SS, Park, JH, et al.. Characterization of increased phenolic compounds from fermented Bokbunja (Rubus coreanus Miq.) and related antioxidant activity. J Pharmaceut Biomed Anal 2009;49:820–7. DOI: https://doi.org/10.1016/j.jpba.2008.12.024.Search in Google Scholar
42. Laaksonen, O, Kuldjarv, R, Paalme, T, Virkki, M, Yang, BR. Impact of apple cultivar, ripening stage, fermentation type and yeast strain on phenolic composition of apple ciders. Food Chem 2017;233:29–37. https://doi.org/10.1016/j.foodchem.2017.04.067.Search in Google Scholar
43. Wang, T, He, FL, Chen, GB. Improving bioaccessibility and bioavailability of phenolic compounds in cereal grains through processing technologies: a concise review. J Funct Foods 2014;7:101–11. https://doi.org/10.1016/j.jff.2014.01.033.Search in Google Scholar
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