Properties of Probiotic Yoghurt with Wolfberry and Its Metabolic Changes of Polyphenolic Compounds

QI Jin; GUO Shuai; CHEN Yanhui; GAO Yan; ZHUANG Jiao; JU Ning

doi:10.13386/j.issn1002-0306.2024060124

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QI Jin, GUO Shuai, CHEN Yanhui, et al. Properties of Probiotic Yoghurt with Wolfberry and Its Metabolic Changes of Polyphenolic Compounds[J]. Science and Technology of Food Industry, 2025, 46(10): 1−9. (in Chinese with English abstract). doi: 10.13386/j.issn1002-0306.2024060124.

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Properties of Probiotic Yoghurt with Wolfberry and Its Metabolic Changes of Polyphenolic Compounds

School of Food Science and Engineering, Ningxia University, Yinchuan 750021, China

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Received Date: June 10, 2024
Available Online: March 20, 2025

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Abstract

In order to explore the effects of lactic acid bacteria on the bioactive substances and in vitro antioxidant capacity of wolfberry yoghurt, Streptococcus thermophilus, Streptococcus thermophilus, Lactobacillus bulgaricus (3:1), Streptococcus thermophilus, Lactobacillus plantarum (1:1), Streptococcus thermophilus, Lactobacillus paracasei (1:1), Streptococcus thermophilus, Lactobacillus bulgaricus, Lactobacillus plantarum (2:1:2), Streptococcus thermophilus, Lactobacillus bulgaricus and Lactobacillus paracasei (2:1:2) were used to prepare wolfberry yoghurt. Results showed that fermentation could increase the content of polyphenols and flavonoids while reducing the content of carotenoids and polysaccharides. Compared to other samples, the wolfberry yogurt sample (SL-Lpc) fermented by Streptococcus thermophilus, Lactobacillus bulgaricus, and Lactobacillus paracasei (mixed in a 2:1:2 ratio) exhibited the highest viable bacterial counts. In the SL-Lpc sample, the content of carotenoids and polysaccharides showed no significant decrease, whereas polyphenol (0.094 mg/mL) and flavonoid (0.169 mg/mL) contents increased by 16.05% and 14.97%, respectively. The DPPH radical scavenging rate, hydroxyl radical scavenging rate, and ABTS⁺ radical scavenging rate reached 96.33%, 84.83%, and 98.37%, respectively. The antioxidant capacity of SL-Lpc was significantly higher than that of other samples (P<0.05). Correlation analysis demonstrated that polyphenolic compounds (including flavonoids) exhibited a significant positive correlation with in vitro antioxidant activity. Metabolomics analysis identified 16 phenolic acid metabolites (10 upregulated, 6 downregulated) and 12 flavonoid metabolites (9 upregulated, 3 downregulated) with differential abundance during fermentation.
- wolfberry,
- probiotics,
- strain compound,
- yoghurt,
- polyphenol compound

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[1]	段昊, 刘改改, 松伟, 等. 枸杞子在我国保健食品中的应用[J]. 食品工业科技,2024,45(6):12−23. [DUAN H, LIU G G, SONG W, et al. Application of fruits of Lycium barharum L. in health food in China[J]. Science and Technology of Food Industry,2024,45(6):12−23.] DUAN H, LIU G G, SONG W, et al. Application of fruits of Lycium barharum L. in health food in China[J]. Science and Technology of Food Industry, 2024, 45（6）: 12−23.
[2]	LIANG J J, LI X H, LEI W Z, et al. Serum metabolomics combined with 16S rRNA sequencing to reveal the effects of Lycium barbarum polysaccharide on host metabolism and gut microbiota[J]. Food Research International,2023,165:112563. doi: 10.1016/j.foodres.2023.112563
[3]	HUANG W Q, ZHAO M W, WANG X Y, et al. Revisiting the structure of arabinogalactan from Lycium barbarum and the impact of its side chain on anti-ageing activity[J]. Carbohydrate Polymers,2022,286:119282. doi: 10.1016/j.carbpol.2022.119282
[4]	LIANG J L, YANG S, LIU Y Y, et al. Characterization and stability assessment of polyphenols bound to Lycium barbarum polysaccharide:Insights from gastrointestinal digestion and colon fermentation[J]. Food Research International,2024,179:114036. doi: 10.1016/j.foodres.2024.114036
[5]	LIU F, LIU X B, ZHOU Y M, et al. Wolfberry-derived zeaxanthin dipalmitate delays retinal degeneration in a mouse model of retinitis pigmentosa through modulating STAT3, CCL2 and MAPK pathways[J]. Journal of Neurochemistry,2021,158(5):1131−1150. doi: 10.1111/jnc.15472
[6]	SHORI A B, ALJOHANI G S, AL-ZAHRANI A J, et al. Viability of probiotics and antioxidant activity of cashew milk-based yogurt fermented with selected strains of probiotic Lactobacillus spp[J]. LWT,2022,153:112482. doi: 10.1016/j.lwt.2021.112482
[7]	GUNENC A, KHOURY C, LEGAULT C, et al. Seabuckthorn as a novel prebiotic source improves probiotic viability in yogurt[J]. LWT-Food Science and Technology,2016,66:490−495. doi: 10.1016/j.lwt.2015.10.061
[8]	ZYGMANTAITĖ G, KERŠIENĖ M, JASUTIENĖ I, et al. Extract isolated from cranberry pomace as functional ingredient in yoghurt production:Technological properties and digestibility studies[J]. LWT,2021,148:111751. doi: 10.1016/j.lwt.2021.111751
[9]	SIGDEL A, OJHA P, KARKI T B. Phytochemicals and syneresis of osmo-dried mulberry incorporated yoghurt[J]. Food Science & Nutrition,2018,6(4):1045−1052.
[10]	WANG Y, QU S J, CHEN M H, et al. Effects of buckwheat milk Co-fermented with two probiotics and two commercial yoghurt strains on gut microbiota and production of short-chain Fatty Acids[J]. Food Bioscience,2023,53:102537. doi: 10.1016/j.fbio.2023.102537
[11]	GOUDA A S, ADBELRUHMAN F G, SABBAH A H, et al. Theoretical benefits of yogurt-derived bioactive peptides and probiotics in COVID-19 patients–A narrative review and hypotheses[J]. Saudi Journal of Biological Sciences,2021,28(10):5897−5905. doi: 10.1016/j.sjbs.2021.06.046
[12]	AZEEZ K A A, AĞÇAM E, KARACA O B, et al. Effects of prickly pear supplementation on physico-chemical, textural, microbiological and sensory characteristics of probiotic set yoghurts[J]. Food Bioscience,2024,60:104513. doi: 10.1016/j.fbio.2024.104513
[13]	FAN X K, SHI Z H, XU J, et al. Characterization of the effects of binary probiotics and wolfberry dietary fiber on the quality of yogurt[J]. Food Chemistry,2023,406:135020. doi: 10.1016/j.foodchem.2022.135020
[14]	VESELÁ K, KUMHEROVÁ M, KLOJDOVÁ I, et al. Selective culture medium for the enumeration of Lactobacillus plantarum in the presence of Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus[J]. LWT,2019,114:108365. doi: 10.1016/j.lwt.2019.108365
[15]	DEMIRCI T, SERT D, AKTAŞ K, et al. Influence of hot and cold break tomato powders on survival of probiotic L. paracasei subsp. paracasei F19, texture profile and antioxidative activity in set-type yoghurts[J]. LWT,2020,118:108855. doi: 10.1016/j.lwt.2019.108855
[16]	KAN X H, YAN Y M, RAN L W, et al. Ultrasonic-assisted extraction and high-speed counter-current chromatography purification of zeaxanthin dipalmitate from the fruits of Lycium barbarum L.[J]. Food Chemistry,2020,310:125854. doi: 10.1016/j.foodchem.2019.125854
[17]	TRIGUEROS L, WOJDYŁO A, SENDRA E. Antioxidant activity and protein–polyphenol interactions in a pomegranate (Punica granatum L.) yogurt[J]. Journal of Agricultural and Food Chemistry,2014,62(27):6417−6425. doi: 10.1021/jf501503h
[18]	WANG M Z, WANG J, FU L L, et al. Degradation of polysaccharides from Lycium barbarum L. leaves improves bioaccessibility and gastrointestinal transport of endogenous minerals[J]. International Journal of Biological Macromolecules,2020,143:76−84. doi: 10.1016/j.ijbiomac.2019.11.243
[19]	朱晓雪, 龚绵红, 杨秉坤, 等. 不同种类及加工方式对杂粮酸奶体外抗氧化活性的比较[J]. 农业工程学报,2023,39(8):268−275. [ZHU X X, GONG M H, YANG B K, et al. Rative study on antioxidant activity of multigrain yoghurt bydifferent types and processing methods of coarse cereals[J]. Transactions of the Chinese Society of Agricultural Engineering,2023,39(8):268−275.] doi: 10.11975/j.issn.1002-6819.202301132 ZHU X X, GONG M H, YANG B K, et al. Rative study on antioxidant activity of multigrain yoghurt bydifferent types and processing methods of coarse cereals[J]. Transactions of the Chinese Society of Agricultural Engineering, 2023, 39（8）: 268−275. doi: 10.11975/j.issn.1002-6819.202301132
[20]	XU K Q, FAN G J, WU C, et al. Preparation of anthocyanin-rich mulberry juice by microwave-ultrasonic combined pretreatment[J]. Food Science and Biotechnology,2022,31(12):1571−1581. doi: 10.1007/s10068-022-01147-3
[21]	孙正霄, 肖顺丽, 刘陆, 等. 枸杞咀嚼片免疫调节及抗氧化活性分析[J]. 中国实验方剂学杂志,2022,28(8):46−53. [SUN Z X, XIAO S L, LIU L, et al. Immunomodulatory and antioxidant activity of gouqi chewable tablets[J]. Chinese Journal of Experimental Traditional Medical Formulae,2022,28(8):46−53.] SUN Z X, XIAO S L, LIU L, et al. Immunomodulatory and antioxidant activity of gouqi chewable tablets[J]. Chinese Journal of Experimental Traditional Medical Formulae, 2022, 28（8）: 46−53.
[22]	CHEN G J, ZHANG S Q, RAN C X, et al. Extraction, characterization and antioxidant activity of water-soluble polysaccharides from Tuber huidongense[J]. International Journal of Biological Macromolecules,2016,91:431−442. doi: 10.1016/j.ijbiomac.2016.05.108
[23]	LIU Y H, LÜ J H, LIU Z B, et al. Integrative analysis of metabolome and transcriptome reveals the mechanism of color formation in pepper fruit (Capsicum annuum L.)[J]. Food Chemistry,2020,306:125629. doi: 10.1016/j.foodchem.2019.125629
[24]	FAN X K, ZHANG A, ZHANG T, et al. Effects of Semen Ziziphi Spinosae extract and binary probiotics co-fermentation on the quality of yogurt and their underlying molecular mechanisms[J]. Food Chemistry:X,2024,21:101191.
[25]	DU H X, WANG X P, YANG H G, et al. Regulation on the quality of yogurt by phenolic fraction of mulberry pomace supplemented before and after fermentation[J]. Food Control,2023,144:109333. doi: 10.1016/j.foodcont.2022.109333
[26]	ISLAM F, KHAN J, ZEHRAVI M, et al. Synergistic effects of carotenoids:Therapeutic benefits on human health[J]. Process Biochemistry,2024,136:254−272. doi: 10.1016/j.procbio.2023.11.033
[27]	HONDA M. Z-Isomers of lycopene and β-carotene exhibit greater skin-quality improving action than their all-E-isomers[J]. Food Chemistry,2023,421:135954. doi: 10.1016/j.foodchem.2023.135954
[28]	LINNEWIEL-HERMONI K, KHANIN M, DANILENKO M, et al. The anti-cancer effects of carotenoids and other phytonutrients resides in their combined activity[J]. Archives of Biochemistry and Biophysics,2015,572:28−35. doi: 10.1016/j.abb.2015.02.018
[29]	雷建武, 米佳, 罗青, 等. 枸杞中类胡萝卜素及体外抗氧化活性研究[J]. 食品工业,2015,36(12):5−8. [LEI J W, MI J, LUO Q, et al. Composition and antioxidant activity of different varieties of lycium[J]. The Food Industry,2015,36(12):5−8.] LEI J W, MI J, LUO Q, et al. Composition and antioxidant activity of different varieties of lycium[J]. The Food Industry, 2015, 36（12）: 5−8.
[30]	PEREIRA A L F, MACIEL T C, RODRIGUES S. Probiotic beverage from cashew apple juice fermented with Lactobacillus casei[J]. Food Research International,2011,44(5):1276−1283. doi: 10.1016/j.foodres.2010.11.035
[31]	BOON C S, MCCLEMENTS D J, WEISS J, et al. Factors influencing the chemical stability of carotenoids in foods[J]. Critical Reviews in Food Science and Nutrition,2010,50(6):515−532. doi: 10.1080/10408390802565889
[32]	段昊, 刘改改, 松伟, 等. 枸杞子在我国保健食品中的应用[J/OL]. 食品工业科技, 1−20[2024-03-06]. https://doi.org/10.13386/j.issn1002-0306.2023060225. [DUAN H, LIU G G, SONG W, et al. Application of fruits of Lycium barharum L. in health food in China[J]. Science and Technology of Food Industry, 1−20[2024-03-06]. https://doi.org/10.13386/j.issn1002-0306.2023060225.] DUAN H, LIU G G, SONG W, et al. Application of fruits of Lycium barharum L. in health food in China[J]. Science and Technology of Food Industry, 1−20[2024-03-06]. https://doi.org/10.13386/j.issn1002-0306.2023060225.
[33]	LIU S, HU J L, ZHONG Y D, et al. A review:Effects of microbial fermentation on the structure and bioactivity of polysaccharides in plant-based foods[J]. Food Chemistry,2024,440:137453. doi: 10.1016/j.foodchem.2023.137453
[34]	QI J, HUANG H, WANG J, et al. Insights into the improvement of bioactive phytochemicals, antioxidant activities and flavor profiles in Chinese wolfberry juice by select lactic acid bacteria[J]. Food Bioscience,2021,43:101264. doi: 10.1016/j.fbio.2021.101264
[35]	KWAW E, MA Y, TCHABO W, et al. Effect of lactobacillus strains on phenolic profile, color attributes and antioxidant activities of lactic-acid-fermented mulberry juice[J]. Food Chemistry,2018,250:148−154. doi: 10.1016/j.foodchem.2018.01.009
[36]	CHENG Z Y, LI Y Z, CHANG W B. Kinetic deoxyribose degradation assay and its application in assessing the antioxidant activities of phenolic compounds in a Fenton-type reaction system[J]. Analytica Chimica Acta,2003,478(1):129−37. doi: 10.1016/S0003-2670(02)01435-6
[37]	SIHAG S, PAL A, RAVIKANT, et al. Antioxidant properties and free radicals scavenging activities of pomegranate (Punica granatum L.) peels:An in vitro study[J]. Biocatalysis and Agricultural Biotechnology,2022,42:102368. doi: 10.1016/j.bcab.2022.102368
[38]	LIZARDO R C M, CHO H D, WON Y S, et al. Fermentation with mono-and mixed cultures of Lactobacillus plantarum and L. casei enhances the phytochemical content and biological activities of cherry silverberry (Elaeagnus multiflora Thunb.) fruit[J]. Journal of the Science of Food and Agriculture,2020,100(9):3687−3696. doi: 10.1002/jsfa.10404
[39]	LIU R Y, LAN H N, LIU Z H, et al. Microbial valorization of lignin toward coumarins:Challenges and perspectives[J]. Renewable and Sustainable Energy Reviews,2024,191:114205. doi: 10.1016/j.rser.2023.114205
[40]	GAUR G, GÄNZLE M G. Conversion of (poly)phenolic compounds in food fermentations by lactic acid bacteria:Novel insights into metabolic pathways and functional metabolites[J]. Current Research in Food Science,2023,6:100448. doi: 10.1016/j.crfs.2023.100448
[41]	XIAO Y, HE C, CHEN Y L, et al. UPLC–QQQ–MS/MS-based widely targeted metabolomic analysis reveals the effect of solid-state fermentation with Eurotium cristatum on the dynamic changes in the metabolite profile of dark tea[J]. Food Chemistry,2022,378:131999. doi: 10.1016/j.foodchem.2021.131999
[42]	NURKENOV O A, FAZYLOV S D, SATPAEVA Z B, et al. Synthesis, structure and biological activity of hydrazones derived from 2- and 4-hydroxybenzoic acid hydrazides[J]. Chemical Data Collections,2023,48:101089. doi: 10.1016/j.cdc.2023.101089
[43]	LOFFT Z, TAIBI A, MASSARA P, et al. Cranberry proanthocyanidin and its microbial metabolite 3, 4-dihydroxyphenylacetic acid, but Not 3-(4-Hydroxyphenyl)-propionic acid, partially reverse pro-inflammatory microRNA responses in human intestinal epithelial cells[J]. Molecular Nutrition & Food Research,2022,66(8):2100853.
[44]	MU W M, YANG Y, JIA J H, et al. Production of 4-hydroxyphenyllactic acid by Lactobacillus sp. SK007 fermentation[J]. Journal of Bioscience and Bioengineering,2010,109(4):369−371. doi: 10.1016/j.jbiosc.2009.10.005
[45]	LUO Z W, LEE S Y. Metabolic engineering of Escherichia coli for the production of benzoic acid from glucose[J]. Metabolic Engineering,2020,62:298−311. doi: 10.1016/j.ymben.2020.10.002
[46]	YUAN K L, WU G K, LI X S, et al. Anthocyanins degradation mediated by β-glycosidase contributes to the color loss during alcoholic fermentation in a structure-dependent manner[J]. Food Research International,2024,175:113732. doi: 10.1016/j.foodres.2023.113732
[47]	SI J Y, XIE J Y, ZHENG B, et al. Release characteristic of bound polyphenols from tea residues insoluble dietary fiber by mixed solid-state fermentation with cellulose degrading strains CZ-6 and CZ-7[J]. Food Research International,2023,173:113319. doi: 10.1016/j.foodres.2023.113319
[48]	LEONARD W, ZHANG P, YING D, et al. Fermentation transforms the phenolic profiles and bioactivities of plant-based foods[J]. Biotechnology Advances,2021,49:107763. doi: 10.1016/j.biotechadv.2021.107763
[49]	JI Z K, DENG W, CHEN D, et al. Recent understanding of the mechanisms of the biological activities of hesperidin and hesperetin and their therapeutic effects on diseases[J]. Heliyon,2024,10(5):e26862. doi: 10.1016/j.heliyon.2024.e26862
[50]	LEE Y S, HUH J Y, NAM S H, et al. Enzymatic bioconversion of citrus hesperidin by Aspergillus sojae naringinase:Enhanced solubility of hesperetin-7-O-glucoside with in vitro inhibition of human intestinal maltase, HMG-CoA reductase, and growth of Helicobacter pylori[J]. Food Chemistry,2012,135(4):2253−2259. doi: 10.1016/j.foodchem.2012.07.007
[51]	CHOI E H, CHUN Y S, KIM J, et al. Modulating lipid and glucose metabolism by glycosylated kaempferol rich roasted leaves of Lycium chinense via upregulating adiponectin and AMPK activation in obese mice-induced type 2 diabetes[J]. Journal of Functional Foods,2020,72:104072. doi: 10.1016/j.jff.2020.104072
[52]	WU W X, LUO X M, WANG Y, et al. Combined metabolomics and transcriptomics analysis reveals the mechanism underlying blue light-mediated promotion of flavones and flavonols accumulation in Ligusticum chuanxiong Hort. microgreens[J]. Journal of Photochemistry and Photobiology B:Biology,2023,242:112692. doi: 10.1016/j.jphotobiol.2023.112692