Polyphenols as a new class of prebiotics for gut microbiota manipulation

  • Ana Bačić University of Belgrade – Innovation Centre of Faculty of Technology and Metallurgy
  • Jelisaveta Gavrilović University in Belgrade – Faculty of Technology and Metallurgy, Department for Biochemical Engineering and Biotechnology
  • Mirjana Rajilić-Stojanović University in Belgrade – Faculty of Technology and Metallurgy, Department for Biochemical Engineering and Biotechnology
Keywords: polyphenols, microbiota, prebiotic, quorum-sensing

Abstract


A thriving community of microorganisms resides in our intestines, forming complex interactions and producing signaling molecules that can affect human physiological processes. Intrinsic and environmental factors modulate the composition of the microbial ecosystem, with diet representing a key factor affecting the formation of gut microbiota. The epidemic of non-communicable chronic diseases has been associated with the Western diet, which may modulate the gut microbiota, resulting in a detrimental derangement in the microbial community, termed dysbiosis. Dysbiosis may be reverted through dietary interventions and the application of probiotics and prebiotics. Phenolic compounds represent plant-based nutraceuticals, which can be separated into phenolic acids and polyphenols, that exert prebiotic-like effects and may prevent the development of diseases. Besides direct health-promoting activities, beneficial effects of phenolic compounds may be exerted through their interaction with the gut microbiota. A bidirectional relationship between the gut microbiota and phenolic compounds has been observed, as microorganisms are involved in the metabolism of phenolic compounds, whereas phenolic compounds may affect the composition of the microbiota, with selective stimulatory or inhibitory activity towards the growth of microbial members. In this review, insight into the gut microbiota-polyphenols relationship will be given, with a focus on the application of polyphenols for modifying microbiota and promoting health.

References

Nazzaro F, Fratianni F, De Feo V, Battistelli A, Da Cruz AG, Coppola R. Chapter Two - Polyphenols, the new frontiers of prebiotics. In: da Cruz AG, Prudencio ES, Esmerino EA, da Silva MC, editors. Advances in Food and Nutrition Research, Volume 94. Academic Press; 2020; p. 35-89.

Thursby E, Juge N. Introduction to the human gut microbiota. Biochem J. 2017;474(11):1823-36.

Yang J, Pu J, Lu S, Bai X, Wu Y, Jin D, et al. Species-Level Analysis of Human Gut Microbiota With Metataxonomics. Front Microbiol. 2020;11:2029.

Berg G, Rybakova D, Fischer D, Cernava T, Vergès M-CC, Charles T, et al. Microbiome definition re-visited: old concepts and new challenges. Microbiome. 2020;8(1):1-22.

Bharti R, Grimm DG. Current challenges and best-practice protocols for microbiome analysis. Brief Bioinform. 2021;22(1):178-93.

Sommer MO. Advancing gut microbiome research using cultivation. Curr Opin Microbiol. 2015;27:127-32.

Pérez JC. Fungi of the human gut microbiota: Roles and significance. Int J Med Microbiol. 2021;311(3):151490.

Cao Z, Sugimura N, Burgermeister E, Ebert MP, Zuo T, Lan P. The gut virome: A new microbiome component in health and disease. EBioMedicine. 2022;81:104113.

Rajilić-Stojanović M, De Vos WM. The first 1000 cultured species of the human gastrointestinal microbiota. FEMS Microbiol Rev. 2014;38(5):996-1047.

Jandhyala SM, Talukdar R, Subramanyam C, Vuyyuru H, Sasikala M, Nageshwar Reddy D. Role of the normal gut microbiota. World J Gastroenterol. 2015;21(29):8787-803.

Liu J, Tan Y, Cheng H, Zhang D, Feng W, Peng C. Functions of gut microbiota metabolites, current status and future perspectives. Aging Dis. 2022;13(4):1106.

Bačić A, Rajilić-Stojanović M. Microbiota changes throughout life-an overview. Comprehensive Gut Microbiota. 2022;2:1-12.

Dueñas M, Muñoz-González I, Cueva C, Jiménez-Girón A, Sánchez-Patán F, Santos-Buelga C, et al. A survey of modulation of gut microbiota by dietary polyphenols. Biomed Res Int. 2015;2015:850902.

Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012;486(7402):222-7.

David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559-63.

Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH. The influence of diet on the gut microbiota. Pharmacol Res. 2013;69(1):52-60.

Jew S, AbuMweis SS, Jones PJ. Evolution of the human diet: linking our ancestral diet to modern functional foods as a means of chronic disease prevention. J Med Food. 2009;12(5):925-34.

Carrera-Bastos P, Fontes-Villalba M, O’Keefe JH, Lindeberg S, Cordain L. The western diet and lifestyle and diseases of civilization. Res Rep Clin Cardiol. 2011;2:15-35.

Sonnenburg ED, Sonnenburg JL. The ancestral and industrialized gut microbiota and implications for human health. Nat Rev Microbiol. 2019;17(6):383-90.

De Filippo C, Di Paola M, Ramazzotti M, Albanese D, Pieraccini G, Banci E, et al. Diet, environments, and gut microbiota. A preliminary investigation in children living in rural and urban Burkina Faso and Italy. Front Microbiol. 2017;8:1979.

Yang Z, Chen Z, Lin X, Yao S, Xian M, Ning X, et al. Rural environment reduces allergic inflammation by modulating the gut microbiota. Gut Microbes. 2022;14(1):2125733.

Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, et al. Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14(8):491-502.

Wang H, Zhao T, Liu Z, Danzengquzhen, Cisangzhuoma, Ma J, et al. The neuromodulatory effects of flavonoids and gut Microbiota through the gut-brain axis. Front Cell Infect Microbiol. 2023;13:1197646.

Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis. 2015;26(1):26191.

Leeming ER, Johnson AJ, Spector TD, Le Roy CI. Effect of Diet on the Gut Microbiota: Rethinking Intervention Duration. Nutrients. 2019;11(12):2862.

Xiao S, Fei N, Pang X, Shen J, Wang L, Zhang B, et al. A gut microbiota-targeted dietary intervention for amelioration of chronic inflammation underlying metabolic syndrome. FEMS Microbiol Ecol. 2014;87(2):357-67.

Sánchez B, Delgado S, Blanco-Míguez A, Lourenço A, Gueimonde M, Margolles A. Probiotics, gut microbiota, and their influence on host health and disease. Mol Nutr Food Res. 2017;61(1):1600240.

Lyu M, Wang Y-f, Fan G-w, Wang X-y, Xu S-y, Zhu Y. Balancing Herbal Medicine and Functional Food for Prevention and Treatment of Cardiometabolic Diseases through Modulating Gut Microbiota. Front Microbiol. 2017;8:2146.

Hutkins RW, Krumbeck JA, Bindels LB, Cani PD, Fahey G, Goh YJ, et al. Prebiotics: why definitions matter. Curr Opin Biotechnol. 2016;37:1-7.

Gibson GR, Scott KP, Rastall RA, Tuohy KM, Hotchkiss A, Dubert-Ferrandon A, et al. Dietary prebiotics: current status and new definition. Food Sci Technol Bull Funct Foods. 2010;7(1):1-19.

Scott KP, Grimaldi R, Cunningham M, Sarbini SR, Wijeyesekera A, Tang MLK, et al. Developments in understanding and applying prebiotics in research and practice—an ISAPP conference paper. J Appl Microbiol. 2020;128(4):934-49.

You S, Ma Y, Yan B, Pei W, Wu Q, Ding C, et al. The promotion mechanism of prebiotics for probiotics: A review. Front Nutr. 2022;9:1000517.

Tungmunnithum D, Thongboonyou A, Pholboon A, Yangsabai A. Flavonoids and Other Phenolic Compounds from Medicinal Plants for Pharmaceutical and Medical Aspects: An Overview. Medicines (Basel). 2018;5(3):93.

Vermerris W, Nicholson R. Families of Phenolic Compounds and Means of Classification. In: Vermerris W, Nicholson R, editors. Phenolic Compound Biochemistry. Dordrecht: Springer Netherlands; 2006; p. 1-34.

de la Rosa LA, Moreno-Escamilla JO, Rodrigo-García J, Alvarez-Parrilla E. Chapter 12 - Phenolic Compounds. In: Yahia EM, editor. Postharvest Physiology and Biochemistry of Fruits and Vegetables. Woodhead Publishing; 2019; p. 253-71.

Al Mamari HH. Phenolic compounds: Classification, chemistry, and updated techniques of analysis and synthesis. In: Badria AF, editor. Phenolic Compounds: Chemistry, Synthesis, Diversity, Non-Conventional Industrial, Pharmaceutical and Therapeutic Applications. Intech; 2021; p. 73-94.

Del Rio D, Rodriguez-Mateos A, Spencer JP, Tognolini M, Borges G, Crozier A. Dietary (poly)phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid Redox Signal. 2013;18(14):1818-92.

Kumar N, Goel N. Phenolic acids: Natural versatile molecules with promising therapeutic applications. Biotechnol Rep (Amst). 2019;24:e00370.

González‐Sarrías A, Tomás‐Barberán FA, García‐Villalba R. Structural diversity of polyphenols and distribution in foods. In: Tomás-Barberán FA, González-Sarrías A, García-Villalba R, editors. Dietary polyphenols: Their metabolism and health effects. John Wiley & Sons; 2020; p. 1-29.

Baky MH, Elshahed M, Wessjohann L, Farag MA. Interactions between dietary flavonoids and the gut microbiome: a comprehensive review. Br J Nutr. 2022;128(4):577-91.

Cortés-Martín A, Selma MV, Tomás-Barberán FA, González-Sarrías A, Espín JC. Where to Look into the Puzzle of Polyphenols and Health? The Postbiotics and Gut Microbiota Associated with Human Metabotypes. Mol Nutr Food Res. 2020;64(9):1900952.

Duda-Chodak A. The inhibitory effect of polyphenols on human gut microbiota. J Physiol Pharmacol. 2012;63(5):497-503.

Ruskovska T, Maksimova V, Milenkovic D. Polyphenols in human nutrition: from the in vitro antioxidant capacity to the beneficial effects on cardiometabolic health and related inter-individual variability - an overview and perspective. Br J Nutr. 2020;123(3):241-54.

Zamora-Ros R, Knaze V, Rothwell JA, Hémon B, Moskal A, Overvad K, et al. Dietary polyphenol intake in Europe: the European Prospective Investigation into Cancer and Nutrition (EPIC) study. Eur J Nutr. 2016;55(4):1359-75.

Godos J, Marventano S, Mistretta A, Galvano F, Grosso G. Dietary sources of polyphenols in the Mediterranean healthy Eating, Aging and Lifestyle (MEAL) study cohort. Int J Food Sci Nutr. 2017;68(6):750-6.

Pérez-Jiménez J, Neveu V, Vos F, Scalbert A. Identification of the 100 richest dietary sources of polyphenols: an application of the Phenol-Explorer database. Eur J Clin Nutr. 2010;64(3):S112-S20.

Rolnik A, Olas B. The Plants of the Asteraceae Family as Agents in the Protection of Human Health. Int J Mol Sci. 2021;22(6).

Chan C-L, Gan R-Y, Corke H. The phenolic composition and antioxidant capacity of soluble and bound extracts in selected dietary spices and medicinal herbs. Int J Food SciTechnol. 2016;51(3):565-73.

Huang W-Y, Cai Y-Z, Zhang Y. Natural phenolic compounds from medicinal herbs and dietary plants: potential use for cancer prevention. Nutr Cancer. 2009;62(1):1-20.

Thumann TA, Pferschy-Wenzig EM, Moissl-Eichinger C, Bauer R. The role of gut microbiota for the activity of medicinal plants traditionally used in the European Union for gastrointestinal disorders. J Ethnopharmacol. 2019;245:112153.

Luca SV, Macovei I, Bujor A, Miron A, Skalicka-Woźniak K, Aprotosoaie AC, et al. Bioactivity of dietary polyphenols: The role of metabolites. Crit Rev Food Sci Nutr. 2020;60(4):626-59.

Zhang L-X, Li C-X, Kakar MU, Khan MS, Wu P-F, Amir RM, et al. Resveratrol (RV): A pharmacological review and call for further research. Biomed Pharmacother. 2021;143:112164.

Oliveira MRd, Nabavi SF, Daglia M, Rastrelli L, Nabavi SM. Epigallocatechin gallate and mitochondria—A story of life and death. Pharmacol Res. 2016;104:70-85.

Sharifi-Rad M, Pezzani R, Redaelli M, Zorzan M, Imran M, Ahmed Khalil A, et al. Preclinical Activities of Epigallocatechin Gallate in Signaling Pathways in Cancer. Molecules. 2020;25(3):467.

Legeay S, Rodier M, Fillon L, Faure S, Clere N. Epigallocatechin Gallate: A Review of Its Beneficial Properties to Prevent Metabolic Syndrome. Nutrients. 2015;7(7):5443-68.

Wan MLY, Co VA, El-Nezami H. Dietary polyphenol impact on gut health and microbiota. Crit Rev Food Sci Nutr. 2021;61(4):690-711.

Muhammad Bilal H, Sadia H, Marwa W, Ahsan J, Muhammad Adil F, Ali T. Bioavailability and Metabolic Pathway of Phenolic Compounds. In: Marcos SH, Rosario GM, Mariana PT, editors. Plant Physiological Aspects of Phenolic Compounds. Rijeka: IntechOpen; 2019; ch. 5.

Tomás-Barberán FA, Selma MV, Espín JC. Interactions of gut microbiota with dietary polyphenols and consequences to human health. Curr Opin Clin Nutr Metab Care. 2016;19(6):471-6.

Zhang M, Cui S, Mao B, Zhang Q, Zhao J, Zhang H, et al. Ellagic acid and intestinal microflora metabolite urolithin A: A review on its sources, metabolic distribution, health benefits, and biotransformation. Crit Rev Food Sci Nutr. 2023;63(24):6900-22.

Rudrapal M, Khairnar SJ, Khan J, Dukhyil AB, Ansari MA, Alomary MN, et al. Dietary Polyphenols and Their Role in Oxidative Stress-Induced Human Diseases: Insights Into Protective Effects, Antioxidant Potentials and Mechanism(s) of Action. Front Pharmacol. 2022;13:806470.

Rudrapal M, Khairnar SJ, Khan J, Dukhyil AB, Ansari MA, Alomary MN, et al. Dietary polyphenols and their role in oxidative stress-induced human diseases: Insights into protective effects, antioxidant potentials and mechanism (s) of action. Front Pharmacol. 2022;13:283.

Shakoor H, Feehan J, Apostolopoulos V, Platat C, Al Dhaheri AS, Ali HI, et al. Immunomodulatory Effects of Dietary Polyphenols. Nutrients. 2021;13(3):728.

Lippolis T, Cofano M, Caponio GR, De Nunzio V, Notarnicola M. Bioaccessibility and Bioavailability of Diet Polyphenols and Their Modulation of Gut Microbiota. Int J Mol Sci. 2023;24(4):3813.

Aravind SM, Wichienchot S, Tsao R, Ramakrishnan S, Chakkaravarthi S. Role of dietary polyphenols on gut microbiota, their metabolites and health benefits. Food Res Int. 2021;142:110189.

Rasheed Z, Akhtar N, Anbazhagan AN, Ramamurthy S, Shukla M, Haqqi TM. Polyphenol-rich pomegranate fruit extract (POMx) suppresses PMACI-induced expression of pro-inflammatory cytokines by inhibiting the activation of MAP Kinases and NF-κB in human KU812 cells. J Inflamm. 2009;6(1):1.

Ozma MA, Khodadadi E, Pakdel F, Kamounah FS, Yousefi M, Yousefi B, et al. Baicalin, a natural antimicrobial and anti-biofilm agent. J Herb Med. 2021;27:100432.

Kim H, Venancio VP, Fang C, Dupont AW, Talcott ST, Mertens-Talcott SU. Mango (Mangifera indica L.) polyphenols reduce IL-8, GRO, and GM-SCF plasma levels and increase Lactobacillus species in a pilot study in patients with inflammatory bowel disease. Nutr Res. 2020;75:85-94.

Fresco P, Borges F, Marques M, Diniz C. The anticancer properties of dietary polyphenols and its relation with apoptosis. Curr Pharm Des. 2010;16(1):114-34.

Selma MV, Espín JC, Tomás-Barberán FA. Interaction between Phenolics and Gut Microbiota: Role in Human Health. J Agric Food Chem. 2009;57(15):6485-501.

Bolca S, Van de Wiele T, Possemiers S. Gut metabotypes govern health effects of dietary polyphenols. Curr Opin Biotechnol. 2013;24(2):220-5.

Tomás-Barberán FA, Selma MV, Espín JC. Interactions of gut microbiota with dietary polyphenols and consequences to human health. Curr Opin Clin Nutr Metab Care. 2016;19(6):471-6.

Alves-Santos AM, Sugizaki CSA, Lima GC, Naves MMV. Prebiotic effect of dietary polyphenols: A systematic review. J Funct Foods. 2020;74:104169.

Fidélix M, Milenkovic D, Sivieri K, Cesar T. Microbiota modulation and effects on metabolic biomarkers by orange juice: A controlled clinical trial. Food Funct. 2020;11(2):1599-610.

Anhê FF, Pilon G, Roy D, Desjardins Y, Levy E, Marette A. Triggering Akkermansia with dietary polyphenols: A new weapon to combat the metabolic syndrome? Gut Microbes. 2016;7(2):146-53.

Rodríguez-Daza MC, de Vos WM. Polyphenols as Drivers of a Homeostatic Gut Microecology and Immuno-Metabolic Traits of Akkermansia muciniphila: From Mouse to Man. Int J Mol Sci. 2022;24(1):45.

Li Z, Henning SM, Lee R-P, Lu Q-Y, Summanen PH, Thames G, et al. Pomegranate extract induces ellagitannin metabolite formation and changes stool microbiota in healthy volunteers. Food Funct. 2015;6(8):2487-95.

González de Llano D, Moreno-Arribas MV, Bartolomé B. Cranberry Polyphenols and Prevention against Urinary Tract Infections: Relevant Considerations. Molecules. 2020;25(15):3523.

LaPlante KL, Sarkisian SA, Woodmansee S, Rowley DC, Seeram NP. Effects of cranberry extracts on growth and biofilm production of Escherichia coli and Staphylococcus species. Phytother Res. 2012;26(9):1371-4.

Duda-Chodak A, Tarko T, Satora P, Sroka P. Interaction of dietary compounds, especially polyphenols, with the intestinal microbiota: a review. Eur J Nutr. 2015;54(3):325-41.

Walker JM, Eckardt P, Aleman JO, da Rosa JC, Liang Y, Iizumi T, et al. The effects of trans-resveratrol on insulin resistance, inflammation, and microbiota in men with the metabolic syndrome: A pilot randomized, placebo-controlled clinical trial. J Clin Transl Res. 2019;4(2):122-35.

Bird JK, Raederstorff D, Weber P, Steinert RE. Cardiovascular and Antiobesity Effects of Resveratrol Mediated through the Gut Microbiota. Adv Nutr. 2017;8(6):839-49.

Chaplin A, Carpéné C, Mercader J. Resveratrol, Metabolic Syndrome, and Gut Microbiota. Nutrients. 2018;10(11):1651.

Kim H, Castellon-Chicas MJ, Arbizu S, Talcott ST, Drury NL, Smith S, et al. Mango (Mangifera indica L.) Polyphenols: Anti-Inflammatory Intestinal Microbial Health Benefits, and Associated Mechanisms of Actions. Molecules. 2021;26(9):2732.

Milutinović M, Dimitrijević-Branković S, Rajilić-Stojanović M. Plant Extracts Rich in Polyphenols as Potent Modulators in the Growth of Probiotic and Pathogenic Intestinal Microorganisms. Front Nutr. 2021;8:688843.

Dmitrieva A, Kozlova O, Atuchin V, Milentieva I, Vesnina A, Ivanova S, et al. Study of the Effect of Baicalin from Scutellaria baicalensis on the Gastrointestinal Tract Normoflora and Helicobacter pylori. Int J Mol Sci. 2023;24(15):11906.

Edwards C, Havlik J, Cong W, Mullen W, Preston T, Morrison D, et al. Polyphenols and health: Interactions between fibre, plant polyphenols and the gut microbiota. Nutr Bull. 2017;42(4):356-360.

De Kievit TR, Iglewski BH. Bacterial quorum sensing in pathogenic relationships. Infection and immunity. 2000;68(9):4839-49.

Nazzaro F, Fratianni F, Coppola R. Quorum sensing and phytochemicals. Int J Mol Sci. 2013;14(6):12607-19.

Rutherford ST, Bassler BL. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med. 2012;2(11):a012427.

González JE, Keshavan ND. Messing with bacterial quorum sensing. Microbiol Mol Biol Rev. 2006;70(4):859-75.

Takó M, Kerekes EB, Zambrano C, Kotogán A, Papp T, Krisch J, et al. Plant phenolics and phenolic-enriched extracts as antimicrobial agents against food-contaminating microorganisms. Antioxidants. 2020;9(2):165.

Zambrano C, Kerekes EB, Kotogán A, Papp T, Vágvölgyi C, Krisch J, et al. Antimicrobial activity of grape, apple and pitahaya residue extracts after carbohydrase treatment against food-related bacteria. LWT. 2019;100:416-25.

Vandeputte OM, Kiendrebeogo M, Rasamiravaka T, Stevigny C, Duez P, Rajaonson S, et al. The flavanone naringenin reduces the production of quorum sensing-controlled virulence factors in Pseudomonas aeruginosa PAO1. Microbiology. 2011;157(7):2120-32.

Zhang J, Rui X, Wang L, Guan Y, Sun X, Dong M. Polyphenolic extract from Rosa rugosa tea inhibits bacterial quorum sensing and biofilm formation. Food Control. 2014;42:125-31.

Yin H, Deng Y, Wang H, Liu W, Zhuang X, Chu W. Tea polyphenols as an antivirulence compound disrupt quorum-sensing regulated pathogenicity of Pseudomonas aeruginosa. Sci Rep. 2015;5(1):16158.

Ponnusamy K, Paul D, Kweon JH. Inhibition of quorum sensing mechanism and Aeromonas hydrophila biofilm formation by vanillin. Environ Eng Sci. 2009;26(8):1359-63.

Published
2023/12/23
Section
Review articles