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Microbial fermentation of blue honeysuckle (Lonicera caerulea L.) polyphenol promotes insulin secretion and intervenes in obesity by promoting short-chain fatty acids production

Fangyi Peia,bXinbo CaoaYanxin RenaLiangyang MaoaYueyi LiuaJingping Gea()Wenxiang Pinga()
Engineering Research Center of Agricultural Microbiology Technology, Ministry of Education & Heilongjiang Provincial Key Laboratory of Ecological Restoration and Resource Utilization for Cold Region & Heilongjiang Provincial Key Laboratory of Plant Genetic Engineering and Biological Fermentation Engineering for Cold Region & Key Laboratory of Microbiology, College of Heilongjiang Province & School of Life Sciences, Heilongjiang University, Harbin 150080, China
Office of Academic Research, Qiqihar Medical University, Qiqihar 161006, China

Peer review under responsibility of Beijing Academy of Food Sciences.

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Highlights

• Blue honeysuckle (BH) polyphenol content increased by 2.63 times after fermentation.

• Seven different polyphenols in FP and UP were significantly promoted SCFAs generation.

• FP and UP on the biosynthesis pathway of SCFAs were different.

• SCFAs had a positive effect on glycolipid metabolism, but LPS had a negative effect.

• FP of BH promoted cells secretion of CCK, GLP-1 and INS, inhibited IL-6 generation.

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Abstract

During obesity treatment, clinicians have been burdened by the ever-increasing number of patients and the side effects of drug treatment. Finding new plant-derived active ingredients as an intervention for obesity has become a research focus. In this study, Plackett-Burman and Central Composite Design experiments, plant-wide target metabolomics technology, simulated human colon fermentation test, and cell experiment in vitro were successively used to investigate the effects of fermented and unfermented polyphenols (FP and UP, respectively) of blue honeysuckle on obesity. After the optimization of the response surface method, polyphenol content ((1878.08 ± 14.53) mg/100 g) increased by 2.63 times after Lactobacillus rhamnosus 6224 and Saccharomyces cerevisiae W5 mixed fermentation. There were 23 significantly different metabolites were observed in FP and UP. Of them, 7 different metabolites were significantly and positively correlated with short-chain fatty acids (SCFAs), whereas negatively correlated with lipopolysaccharides (LPS). The contents of these 7 metabolites were significantly increased in FP. Furthermore, the effects of FP and UP on the SCFA biosynthesis pathway were different. Cell experiments revealed that polyphenols can significantly promote the secretion of gastrointestinal endogenous hormones and insulin and inhibit interleukin-6 levels. Linear regression analysis revealed SCFAs had a positive regulatory effect on glycolipid metabolism, whereas LPS had a negative effect. Overall, these crucial findings provide an economical and simple method for obtaining blue honeysuckle polyphenols and laying a theoretical foundation for its application in the therapeutic intervention against obesity.

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References

[1]

J.F. Geng, Q.Q. Ni, W. Sun, et al., The links between gut microbiota and obesity and obesity related diseases, Biomed Pharmacother. 147 (2022) 112678. https://doi.org/10.1016/j.biopha.2022.112678.

[2]

M.E. Piché, A. Tchernof, J.P, Després, Obesity phenotypes, diabetes, and cardiovascular diseases, Circ. Res. 126 (2020) 1477-1500. https://doi.org/10.1161/CIRCRESAHA.120.316101.

[3]

J. Aaseth, S. Ellefsen, U. Alehagen, et al., Diets and drugs for weight loss and health in obesity – an update, Biomed Pharmacother. 140 (2021) 111789. https://doi.org/10.1016/j.biopha.2021.111789.

[4]

T.D. Zou, F. Xie, P.B. Liang, et al., Polysaccharide-rich fractions from Enteromorpha prolifera improve hepatic steatosis and gut barrier integrity in high-fat diet-induced obese mice linking to modulation of gut microbiota, Biomed. Pharmacother. 157 (2023) 114034. https://doi.org/10.1016/j.biopha.2022.114034.

[5]

P. Chen, S. Lei, M. Tong, et al., Effect of polysaccharide fractions from Fortunella margarita on the fecal microbiota of mice and SCFA production in vitro, Food Sci. Hum. Wellness 11 (2022) 97-108. http://doi.org/10.1016/j.fshw.2021.07.011.

[6]

J.A. Molina-Tijeras, P. Diez-Echave, T. Vezza, et al., Lactobacillus fermentum CECT5716 ameliorates high fat diet-induced obesity in mice through modulation of gut microbiota dysbiosis, Pharmacol. Res. 167 (2021) 105471. https://doi.org/10.1016/j.phrs.2021.105471.

[7]

R. Kowalski, E. Gonzalez de Mejia, Phenolic composition, antioxidant capacity and physical characterization of ten blackcurrant (Ribes nigrum) cultivars, their juices, and the inhibition of type 2 diabetes and inflammation biochemical markers, Food Chem. 359 (2021) 129889. https://doi.org/10.1016/j.foodchem.2021.129889.

[8]

W.W. Sung, J.H. Tu, J.S. Yu, et al., Bacillus amyloliquefaciens exopolysaccharide preparation induces glucagon-like peptide 1 secretion through the activation of bitter taste receptors, Int. J. biol. macromol. 185 (2021) 562-571. https://doi.org/10.1016/j.ijbiomac.2021.06.187.

[9]

T.A.F. Correa, M.M. Rogero, N.M.A. Hassimotto, et al., The two-way polyphenols-microbiota interactions and their effects on obesity and related metabolic diseases, Front. nutr. 6 (2019) 188. https://doi.org/10.3389/fnut.2019.00188.

[10]

Y.B. Kang, X. Kang, H. Yang, et al., Lactobacillus acidophilus ameliorates obesity in mice through modulation of gut microbiota dysbiosis and intestinal permeability, Pharmacol. Res. 175 (2022) 106020. https://doi.org/10.1016/j.phrs.2021.106020.

[11]

P. Louis, G.L. Hold, H.J. Flint, The gut microbiota, bacterial metabolites and colorectal cancer, Nat. Rev. Microbiol. 12 (2014) 661-672. https://doi.org/10.1038/nrmicro3344.

[12]

R.M. Wang, L. Wang, S.W. Wang, et al., Phenolics from noni (Morinda citrifolia L.) fruit alleviate obesity in high fat diet-fed mice via modulating the gut microbiota and mitigating intestinal damage, Food Chem. 402 (2023) 134232. https://doi.org/10.1016/j.foodchem.2022.134232.

[13]

Y.H. Wang, N.X. Gao, A. Nieto-Veloza, et al., Lonicera caerulea polyphenols inhibit fat absorption by regulating Nrf2-ARE pathway mediated epithelial barrier dysfunction and special microbiota, Food Sci. Hum. Wellness 12 (2023) 1309-1322. http://doi.org/10.1016/j.fshw.2022.10.013.

[14]

D.D. Zhou, A. Saimaiti, M. Luo, et al., Fermentation with tea residues enhances antioxidant activities and polyphenol contents in Kombucha beverages, Antioxidants 11 (2022) 155. https://doi.org/10.3390/antiox11010155.

[15]

S.K. Chang, C. Alasalvar, F. Shahidi, Superfruits: phytochemicals, antioxidant efficacies, and health effects - a comprehensive review, Crit. Rev. Food Sci. 59 (2019) 1580-1604. https://doi.org/10.1080/10408398.2017.1422111.

[16]

A. Sharma, H.J. Lee, Lonicera caerulea: An updated account of its phytoconstituents and health-promoting activities, Trends Food Sci. Tech. 107 (2021) 130-149. https://doi.org/10.1016/j.tifs.2020.08.013.

[17]

F.F. de Araujo, D. de Paulo Farias, I.A. Neri-Numa, et al., Polyphenols and their applications: an approach in food chemistry and innovation potential, Food Chem. 338 (2021) 127535. https://doi.org/10.1016/j.foodchem.2020.127535.

[18]

G. Catalkaya, K. Venema, L. Lucini, et al., Interaction of dietary polyphenols and gut microbiota: microbial metabolism of polyphenols, influence on the gut microbiota, and implications on host health, Food Front. 1 (2020) 109-133. https://doi.org/10.1002/fft2.25.

[19]

G.B. Celli, A. Ghanem, M.S.L. Brooks, Haskap berries (Lonicera caerulea L.)—a critical review of antioxidant capacity and health-related studies for potential value-added products, Food Bioprocess Technol. 7 (2014) 1541-1554. https://doi.org/10.1007/s11947-014-1301-2.

[20]

T. Jurikova, O. Rop, J. Mlcek, et al., Phenolic profile of edible honeysuckle berries (genus Lonicera) and their biological effects, Molecules 17 (2011) 61-79. https://doi.org/10.3390/molecules17010061.

[21]

E. Kwaw, Y.K. Ma, W. Tchabo, et al., Effect of lactobacillus strains on phenolic profile, color attributes and antioxidant activities of lactic-acid-fermented mulberry juice, Food Chem. 250 (2018) 148-154. https://doi.org/10.1016/j.foodchem.2018.01.009.

[22]

G. Dominguez-Rodriguez, M.L. Marina, M. Plaza, Enzyme-assisted extraction of bioactive non-extractable polyphenols from sweet cherry (Prunus avium L.) pomace, Food Chem. 339 (2021) 128086. https://doi.org/10.1016/j.foodchem.2020.128086.

[23]

S.W. Sun, S.Q. Huang, Y.N. Shi, et al., Extraction, isolation, characterization and antimicrobial activities of non-extractable polyphenols from pomegranate peel, Food Chem. 351 (2021) 129232. https://doi.org/10.1016/j.foodchem.2021.129232.

[24]

W.J. Song, V. Lagmay, B.G. Jeong, et al., Changes in physicochemical and functional properties of Opuntia humifusa during fermentation with cellulolytic enzyme and lactic acid bacteria, LWT-Food Sci. Technol. 159 (2022) 113192. https://doi.org/10.1016/j.lwt.2022.113192.

[25]

Y.Q. Xu, Y. Zhu, X.T. Li, et al., Dynamic balancing of intestinal short-chain fatty acids: the crucial role of bacterial metabolism, Trends Food Sci. Tech. 100 (2020) 118-130. https://doi.org/10.1016/j.tifs.2020.02.026.

[26]

B.T. Oh, S.Y. Jeong, P. Velmurugan, et al., Probiotic-mediated blueberry (Vaccinium corymbosum L.) fruit fermentation to yield functionalized products for augmented antibacterial and antioxidant activity, J. Biosci. Bioeng. 124 (2017) 542-550. http://doi.org/10.1016/j.jbiosc.2017.05.011.

[27]

S.J. Li, Y. Tao, D.D. Li, et al., Fermentation of blueberry juices using autochthonous lactic acid bacteria isolated from fruit environment: fermentation characteristics and evolution of phenolic profiles, Chemosphere 276 (2021) 130090. https://doi.org/10.1016/j.chemosphere.2021.130090.

[28]

B. de la Fuente, C. Luz, C. Puchol, et al., Evaluation of fermentation assisted by Lactobacillus brevis POM, and Lactobacillus plantarum (TR-7, TR-71, TR-14) on antioxidant compounds and organic acids of an orange juice-milk based beverage, Food Chem. 343 (2021) 128414. https://doi.org/10.1016/j.foodchem.2020.128414.

[29]

L. Wang, Q. Bei, Y.N. Wu, et al., Characterization of soluble and insoluble-bound polyphenols from Psidium guajava L. leaves co-fermented with Monascus anka and Bacillus sp. and their bio-activities, J. Funct. Foods 32 (2017) 149-159. http://doi.org/10.1016/j.jff.2017.02.029.

[30]

D.D. He, S.L. Zheng, J. Xiao, et al., Effect of lignin on short-chain fatty acids production from anaerobic fermentation of waste activated sludge, Water Res. 212 (2022) 118082. https://doi.org/10.1016/j.watres.2022.118082.

[31]

E. de Lourdes Chaves Macêdo, T. Colombo Pimentel, D. de Sousa Melo, et al., Yeasts from fermented Brazilian fruits as biotechnological tools for increasing phenolics bioaccessibility and improving the volatile profile in derived pulps, Food Chem. 401 (2022) 134200. https://doi.org/10.1016/j.foodchem.2022.134200.

[32]

R.D. Cagno, P. Filannino, M. Gobbetti, Lactic acid fermentation drives the optimal volatile flavor-aroma profile of pomegranate juice, Int. J. Food Microbiol. 248 (2017) 56-62. http://doi.org/10.1016/j.ijfoodmicro.2017.02.014.

[33]

W. Zhong, S.Q. Liu, H. Yang, et al., Effect of selected yeast on physicochemical and oenological properties of blueberry wine fermented with citrate-degrading Pichia fermentans, LWT-Food Sci. Technol. 145 (2021) 111261. https://doi.org/10.1016/j.lwt.2021.111261.

[34]

Y. Iqbal, E.N. Ponnampalam, H.A.R. Suleria, et al., LC-ESI/QTOF-MS profiling of chicory and lucerne polyphenols and their antioxidant activities, Antioxidants 10 (2021) 932. https://doi.org/10.3390/antiox10060932.

[35]

M. Berenguer, S. Vegara, E. Barrajon, et al., Physicochemical characterization of pomegranate wines fermented with three different Saccharomyces cerevisiae yeast strains, Food Chem. 190 (2016) 848-855. http://doi.org/10.1016/j.foodchem.2015.06.027.

[36]

Y.H. Wang, J.Y. Zhu, X.J. Meng, et al., Comparison of polyphenol, anthocyanin and antioxidant capacity in four varieties of Lonicera caerulea berry extracts, Food Chem. 197 (2016) 522-529. http://doi.org/10.1016/j.foodchem.2015.11.006.

[37]

X.Y. Zhang, J. Chen, X.L. Li, et al., Dynamic changes in antioxidant activity and biochemical composition of tartary buckwheat leaves during Aspergillus niger fermentation, J. Funct. Foods 32 (2017) 375-381. http://doi.org/10.1016/j.jff.2017.03.022.

[38]

Y. Zhang, W.P. Liu, Z.H. Wei, et al., Enhancement of functional characteristics of blueberry juice fermented by Lactobacillus plantarum, LWT-Food Sci. Technol. 139 (2021) 110590. https://doi.org/10.1016/j.lwt.2020.110590.

[39]

S.W. Liu, J.C. Yu, S. Guo, et al., Inhibition of pancreatic α-amylase by Lonicera caerulea berry polyphenols in vitro and their potential as hyperglycemic agents, LWT-Food Sci. Technol. 126 (2020) 109288. https://doi.org/10.1016/j.lwt.2020.109288.

[40]

F.Y. Pei, X.B. Cao, X.M. Wang, et al., Structural characteristics and bioactivities of polysaccharides from blue honeysuckle after probiotic fermentation, LWT-Food Sci. Technol. 165 (2022) 113764. https://doi.org/10.1016/j.lwt.2022.113764.

[41]

R.P. Du, H.X. Xing, Y.P. Yang, et al., Optimization, purification and structural characterization of a dextran produced by L. mesenteroides isolated from Chinese sauerkraut, Carbohyd Polym. 174 (2017) 409-416. https://doi.org/10.1016/j.carbpol.2017.06.084.

[42]

L.N. Liu, J.J. Xu, R.P. Du, et al., The response surface optimization of exopolysaccharide produced by Saccharomyces cerevisiae Y3 and its partial characterization, Prep. Biochem. Biotech. 52 (2021) 566-577. https://doi.org/10.1080/10826068.2021.1972428.

[43]

Y. Wang, R.P. Du, X.X. Qiao, et al., Optimization and characterization of exopolysaccharides with a highly branched structure extracted from Leuconostoc citreum B-2, Int. J. Biol. Macromol. 142 (2020) 73-84. https://doi.org/10.1016/j.ijbiomac.2019.09.071.

[44]

C. Royo, Y. Ferradas, J.M. Martinez-Zapater, et al., Characterization of Tempranillo negro (VN21), a high phenolic content grapevine Tempranillo clone, through UHPLC-QqQ-MS/MS polyphenol profiling, Food Chem. 360 (2021) 130049. https://doi.org/10.1016/j.foodchem.2021.130049.

[45]

D. Pang, L.J. You, T. Li, et al., Phenolic profiles and chemical- or cell-based antioxidant activities of four star fruit (Averrhoa carambola) cultivars, RSC Adv. 6 (2016) 90646-90653. https://doi.org/10.1039/c6ra15692d.

[46]

F. Pei, W. Li, X.L. Ni, et al., Effect of cooked rice with added fructo-oligosaccharide on faecal microorganisms investigated by in vitro digestion and fermentation, Food Sci. Hum. Wellness 12 (2023) 662-668. https://doi.org/10.1016/j.fshw.2022.07.068.

[47]

A. Burgos-Edwards, A. Fernandez-Romero, M. Carmona, et al., Effects of gastrointestinal digested polyphenolic enriched extracts of Chilean currants (Ribes magellanicum and Ribes punctatum) on in vitro fecal microbiota, Food Res. Int. 129 (2020) 108848. https://doi.org/10.1016/j.foodres.2019.108848.

[48]

Y.Z. Zhu, J.M. Zhou, W. Liu, et al., Effects of exopolysaccharide from Lactobacillus rhamnosus on human gut microbiota in in vitro fermentation model, LWT-Food Sci. Technol. 139 (2021) 110524. https://doi.org/10.1016/j.lwt.2020.110524.

[49]

D. Ashley, D. Marasini, C. Brownmiller, et al., Impact of grain sorghum polyphenols on microbiota of normal weight and overweight/obese subjects during in vitro fecal fermentation, Nutrients 11 (2019) 217. https://doi.org/10.3390/nu11020217.

[50]

Y.A. Chait, A. Gunenc, F. Bendali, et al., Simulated gastrointestinal digestion and in vitro colonic fermentation of carob polyphenols: bioaccessibility and bioactivity, LWT-Food Sci. Technol. 117 (2020) 108623. https://doi.org/10.1016/j.lwt.2019.108623.

[51]

T. Xia, W.H. Duan, Z.J. Zhang, et al., Polyphenol-rich extract of Zhenjiang aromatic vinegar ameliorates high glucose-induced insulin resistance by regulating JNK-IRS-1 and PI3K/Akt signaling pathways, Food Chem. 335 (2021) 127513. https://doi.org/10.1016/j.foodchem.2020.127513.

[52]

J.M. Chen, M.C. Wang, P. Zhang, et al., Cordycepin alleviated metabolic inflammation in Western diet-fed mice by targeting intestinal barrier integrity and intestinal flora, Pharmacol. Res. 178 (2022) 106191. https://doi.org/10.1016/j.phrs.2022.106191.

[53]

C.R. Bae, Y.G. Kwon, CU06-1004 modulates the adenosine monophosphate (AMP)-associated protein kinase (AMPK) signaling pathway and inhibits lipogenesis in 3T3-L1 adipocytes and high-fat diet-induced obese mice, Life Sci. 296 (2022) 120440. https://doi.org/10.1016/j.lfs.2022.120440.

[54]

X.F. Deng, B. Chen, Q. Luo, et al., Hulless barley polyphenol extract inhibits adipogenesis in 3T3-L1 cells and obesity related-enzymes, Front. Nutr. 9 (2022) 933068. https://doi.org/10.3389/fnut.2022.933068.

[55]

R.R. Li, Z.X. Wang, K.W. Kong, et al., Probiotic fermentation improves the bioactivities and bioaccessibility of polyphenols in Dendrobium officinale under in vitro simulated gastrointestinal digestion and fecal fermentation, Front. Nutr. 9 (2022) 1005912. https://doi.org/10.3389/fnut.2022.1005912.

[56]

E.E. Canfora, R.C.R. Meex, K. Venema, et al., Gut microbial metabolites in obesity, NAFLD and T2DM, Nat. Rev. Endocrinol. 15(5) (2019) 261-273. https://doi.org/10.1038/s41574-019-0156-z.

[57]

M.E. Piche, A. Tchernof, J.P. Despres, Obesity phenotypes, diabetes, and cardiovascular diseases, Circ. Res. 126(11) (2020) 1477-1500. https://doi.org/10.1161/CIRCRESAHA.120.316101.

[58]

K. Papoutsis, J.Y. Zhang, M.C. Bowyer, et al., Fruit, vegetables, and mushrooms for the preparation of extracts with α-amylase and α-glucosidase inhibition properties: a review, Food Chem. 338 (2021) 128119. https://doi.org/10.1016/j.foodchem.2020.128119.

[59]

M.L. Clodoveo, P. Crupi, M. Muraglia, et al., Ultrasound assisted extraction of polyphenols from ripe carob pods (Ceratonia siliqua L.): combined designs for screening and optimizing the processing parameters, Foods 11(3) (2022) 284. https://doi.org/10.3390/foods11030284.

[60]

F.F. Li, H.T. Zhao, R.R. Xu, et al., Simultaneous optimization of the acidified water extraction for total anthocyanin content, total phenolic content, and antioxidant activity of blue honeysuckle berries (Lonicera caerulea L.) using response surface methodology, Food Sci Nutr. 7(9) (2019) 2968-2976. https://doi.org/10.1002/fsn3.1152.

[61]

D. Pinto, E.F. Vieira, A.F. Peixoto, et al., Optimizing the extraction of phenolic antioxidants from chestnut shells by subcritical water extraction using response surface methodology, Food Chem. 334 (2021) 127521. https://doi.org/10.1016/j.foodchem.2020.127521.

[62]

Z.R. Ouyang, X.R. Niu, W.G. Wang, et al., The role of short-chain fatty acids in Clostridioides difficile infection: a review, Anaerobe 75 (2022) 102585. https://doi.org/10.1016/j.anaerobe.2022.102585.

Food Science and Human Wellness
Article number: 9250091
Cite this article:
Pei F, Cao X, Ren Y, et al. Microbial fermentation of blue honeysuckle (Lonicera caerulea L.) polyphenol promotes insulin secretion and intervenes in obesity by promoting short-chain fatty acids production. Food Science and Human Wellness, 2025, 14(4): 9250091. https://doi.org/10.26599/FSHW.2024.9250091
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