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Effect of fermentation on antioxidant, antimicrobial, anti-inflammatory, and anti-Helicobacter pylori adhesion activity of Ulmus davidiana var. japonica root bark

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Abstract

The limited yield of Ulmus davidiana var. japonica root bark (URB) extract is considered an economic loss to the food industry. Improving extraction yield and bioactivity through fermentation increase the industrial usage of URB. The study aims to optimize the fermentation with cellulolytic and pectinolytic bacteria and evaluate the bioactivity and anti-Helicobacter pylori activity of the fermented URB extract. URB fermentation with the Bacillus licheniformis FLa3, isolated from salted seafood (Sardinella zunasi), under optimal conditions (37 °C, pH 6, 10% inoculum dose, and 36 h) improved the extraction yield by 36% compared to the control. The antioxidant and antimicrobial activity of the fermented extract were significantly higher than non-fermented extract. High-performance liquid chromatography results confirmed that the fermentation increased the proportion of bioactive components such as catechin (171.7%), epicatechin (144.3%), quercetin (27.3%), and kaempferol (16.7%). The results confirmed that the fermentation increased both the extraction yield and bioactivity.

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References

  • Acosta-Estrada BA, Gutierrez-Uribe JA, Serna-Saldivar SO. Bound phenolics in foods, a review. Food Chemistry. 152: 46-55 (2014)

    Article  CAS  PubMed  Google Scholar 

  • Ajila CM, Brar SK, Verma M, Tyagi RD, Valéro JR. Solid-state fermentation of apple pomace using Phanerocheate chrysosporium-liberation and extraction of phenolic antioxidants. Food Chemistry. 126: 1071-1080 (2011)

    Article  CAS  Google Scholar 

  • Aslam F, Ansari A, Aman A, Baloch G, Nisar G, Baloch AH, Rehman HU. Production of commercially important enzymes from Bacillus licheniformis KIBGE-IB3 using date fruit wastes as substrate. Journal of Genetic Engineering and Biotechnology. 18: 46 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhadrecha P, Bala M, Khasa YP, Arshi A, Singh J, Kumar M. Hippophae rhamnoides L. rhizobacteria exhibit diversified cellulase and pectinase activities. Physiology and Molecular Biology of Plants. 26: 1075-1085 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Butkovic V, Klasinc L, Bors W. Kinetic study of flavonoid reactions with stable radicals. Journal of Agricultural and Food Chemistry. 52: 2816-2820 (2004)

    Article  CAS  PubMed  Google Scholar 

  • Calabriso N, Scoditti E, Massaro M, Pellegrino M, Storelli C, Ingrosso I, Giovinazzo G, Carluccio MA. Multiple anti-inflammatory and anti-atherosclerotic properties of red wine polyphenolic extracts: differential role of hydroxycinnamic acids, flavonols and stilbenes on endothelial inflammatory gene expression. European Journal of Nutrition. 55: 477–489 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Djekic A, Muller A. The immunomodulator VacA promotes immune tolerance and persistent Helicobacter pylori infection through its activities on T-cells and antigen-presenting cells. Toxins (Basel). 8: 187 (2016)

    Article  PubMed  Google Scholar 

  • Escandón RA, del Campo M, López-Solis R, Obreque-Slier E, Toledo H. Antibacterial effect of kaempferol and (-)-epicatechin on Helicobacter pylori. European Food Research and Technology. 242: 1495–1502 (2016)

    Article  Google Scholar 

  • Ferreira Junior M, Batista SA, Vidigal PV, Cordeiro AA, Oliveira FM, Prata LO, Diniz AE, Barral CM, Barbuto RC, Gomes AD, Araujo ID, Queiroz DM, Caliari MV. Infection with CagA-positive Helicobacter pylori strain containing three EPIYA C phosphorylation sites is associated with more severe gastric lesions in experimentally infected mongolian gerbils (Meriones unguiculatus). European Journal of Histochemistry. 59: 2489 (2015)

    CAS  PubMed  Google Scholar 

  • Ghandahari Yazdi AP, Barzegar M, Sahari MA, Ahmadi Gavlighi H. Optimization of the enzyme-assisted aqueous extraction of phenolic compounds from pistachio green hull. Food Science and Nutrition. 7: 356-366 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Graham DY. Helicobacter pylori update: gastric cancer, reliable therapy, and possible benefits. Gastroenterology. 148: 719-31 e3 (2015)

    Article  PubMed  Google Scholar 

  • Jain P, Luo ZQ, Blanke SR. Helicobacter pylori vacuolating cytotoxin A (VacA) engages the mitochondrial fission machinery to induce host cell death. Proceedings of the National Academy of Sciences. 108: 16032-7 (2011)

    Article  CAS  Google Scholar 

  • Kalali B, Mejias-Luque R, Javaheri A, Gerhard M. H. pylori virulence factors: influence on immune system and pathology. Mediators of Inflammation. 2014: 426309 (2014)

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim MJ, Lim SJ, Kang DK. Isolation of a Bacillus licheniformis DK42 producing cellulase and xylanase, and properties of the enzymes. Journal of Animal Science and Technology. 50: 429-436 (2008)

    Article  CAS  Google Scholar 

  • Lee SW, Lim JM, Mohan H, Seralathan KK, Park YJ, Lee JH, Oh BT. Enhanced bioactivity of Zanthoxylum schinifolium fermented extract: anti-inflammatory, anti-bacterial, and anti-melanogenic activity. Journal of Bioscience and Bioengineering. 129: 638-645 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Yu JS, Phung HM, Lee JG, Kim KH, Kang KS. Potential anti-skin aging effect of (-)-catechin isolated from the root bark of Ulmus davidiana var. japonica in tumor necrosis factor-alpha-stimulated normal human dermal fibroblasts. Antioxidants. 9 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leonard W, Zhang P, Ying D, Fang Z. Lignanamides: sources, biosynthesis and potential health benefits - a minireview. Critical Reviews in Food Science and Nutrition. 61: 1404-1414 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Liang Y, Feng Z, Yesuf J, Blackburn JW. Optimization of growth medium and enzyme assay conditions for crude cellulases produced by a novel thermophilic and cellulolytic bacterium, Anoxybacillus sp. 527. Applied Biochemistry and Biotechnology. 160: 1841-1852 (2009)

    Article  PubMed  Google Scholar 

  • Lu MC, Chiu HF, Lin CP, Shen YC, Venkatakrishnan K, Wang CK. Anti-Helicobacter pylori effect of various extracts of ixeris chinensis on inflammatory markers in human gastric epithelial AGS cells. Journal of Herbal Medicine. 11: 60-70 (2018)

    Article  Google Scholar 

  • Ma Y, Ding S, Fei Y, Liu G, Jang H, Fang J. Antimicrobial activity of anthocyanins and catechins against foodborne pathogens Escherichia coli and Salmonella. Food Control. 106: 106712 (2019)

    Article  CAS  Google Scholar 

  • Madeira Junior JV, Teixeira CB, Macedo GA. Biotransformation and bioconversion of phenolic compounds obtainment: an overview. Critical Reviews in Biotechnology. 35: 75-81 (2015)

    Article  PubMed  Google Scholar 

  • Meini MR, Cabezudo I, Boschetti CE, Romanini D. Recovery of phenolic antioxidants from syrah grape pomace through the optimization of an enzymatic extraction process. Food Chemistry. 283: 257-264 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Muller HE. Detection of hydrogen peroxide produced by microorganisms on an ABTS peroxidase medium. Zentralbl Bakteriol Mikrobiol Hyg A. 259: 151-4 (1985)

    CAS  PubMed  Google Scholar 

  • Ngnameko CR, Njayou FN, Fowora M, Nemg FBS, Fewou PM, Smith SI. Inhibitory effect of medicinal plants from cameroon on the growth and adhesion of Helicobacter pylori. European Journal of Integrative Medicine. 30: 100957 (2019)

    Article  Google Scholar 

  • Rieder G, Fischer W, Haas R. Interaction of Helicobacter pylori with host cells: function of secreted and translocated molecules. Current Opinion in Microbiology. 8: 67-73 (2005)

    Article  CAS  PubMed  Google Scholar 

  • Russo M, Spagnuolo C, Tedesco I, Bilotto S, Russo GL. The flavonoid quercetin in disease prevention and therapy: facts and fancies. Biochemical Pharmacology. 83: 6-15 (2012)

    Article  CAS  PubMed  Google Scholar 

  • Saavedra JM, Bauman N, Perman J, Yolken R, Oung I. Feeding of Bifidobacterium bifidum and Streptococcus thermophilus to infants in hospital for prevention of diarrhoea and shedding of rotavirus. Lancet. 344: 1046-1049 (1994)

    Article  CAS  Google Scholar 

  • Saha K, Lajis NH, Israf DA, Hamzah AS, Khozirah S, Khamis S, Syahida A. Evaluation of antioxidant and nitric oxide inhibitory activities of selected malaysian medicinal plants. Journal of Ethnopharmacology. 92: 263-267 (2004)

    Article  CAS  PubMed  Google Scholar 

  • Sethi S, Datta A, Gupta BL, Gupta S. Optimization of cellulase production from bacteria isolated from soil. ISRN Biotechnology. 2013: 985685 (2013)

    Article  PubMed  PubMed Central  Google Scholar 

  • So HM, Yu JS, Khan Z, Subedi L, Ko YJ, Lee IK, Park WS, Chung SJ, Ahn MJ, Kim SY, Kim KH. Chemical constituents of the root bark of Ulmus davidiana var. japonica and their potential biological activities. Bioorganic Chemistry. 91: 103145 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Suerbaum S, Michetti P. Helicobacter pylori infection. The New England Journal of Medicine. 347: 1175-86 (2002)

    Article  CAS  PubMed  Google Scholar 

  • Tamang JP, Watanabe K, Holzapfel WH. Review: diversity of microorganisms in global fermented foods and beverages. Frontiers in Microbiology. 7: 377 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  • Thung I, Aramin H, Vavinskaya V, Gupta S, Park JY, Crowe SE, Valasek MA. Review article: the global emergence of Helicobacter pylori antibiotic resistance. Aliment. Pharmacology and Therapeutics. 43: 514-33 (2016)

    Article  CAS  Google Scholar 

  • Yeon MJ, Lee MH, Kim DH, Yang JY, Woo HJ, Kwon HJ, Moon C, Kim SH, Kim JB. Anti-inflammatory effects of kaempferol on Helicobacter pylori-induced inflammation. Bioscience, Biotechnology, and Biochemistry. 83: 166-173 (2019)

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a grant from the Honam National Institute of Biological Resources (HNIBR), funded by the Ministry of Environment (MOE) of the Republic of Korea (HNIBR202102121).

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Author notes

  1. Seong-Hyeon Lee and Jeong-Muk Lim are co-first authors.

Authors and Affiliations

  1. Division of Biotechnology, Advanced Institute of Environment and Bioscience, College of Environmental and Bioresource Sciences, Jeonbuk National University, Iksan, Jeonbuk, 54596, South Korea

    Seong-Hyeon Lee, Jeong-Muk Lim, Se-Won Lee, Tae-Hu Jang, Jung-Hee Park, Kamala-Kannan Seralathan & Byung-Taek Oh

  2. R&D Center, Sanigen CO., Ltd., Iksan, Jeonbuk, 54576, South Korea

    Young-Seok Seo

  3. Sunchang Research Institute of Health and Longevity, Sunchang, Jeonbuk, 56015, South Korea

    Jeong-Ho Lee

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  1. Seong-Hyeon Lee
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Lee, SH., Lim, JM., Lee, SW. et al. Effect of fermentation on antioxidant, antimicrobial, anti-inflammatory, and anti-Helicobacter pylori adhesion activity of Ulmus davidiana var. japonica root bark. Food Sci Biotechnol 32, 1257–1268 (2023). https://doi.org/10.1007/s10068-023-01259-4

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