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      Metabolomics reveals impact of seven functional foods on metabolic pathways in a gut microbiota model

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          Highlights

          • Metabolomics was employed to assess 7 functional foods impact on gut microbiota.

          • Insights regarding how functional foods alter gut metabolic pathways is presented.

          • Increased GABA production was observed in polyphenol rich functional food.

          • Purine alkaloids served as direct substrate in microbiota metabolism.

          Abstract

          Functional food defined as dietary supplements that in addition to their nutritional values, can beneficially modulate body functions becomes more and more popular but the reaction of the intestinal microbiota to it is largely unknown. In order to analyse the impact of functional food on the microbiota itself it is necessary to focus on the physiology of the microbiota, which can be assessed in a whole by untargeted metabolomics. Obtaining a detailed description of the gut microbiota reaction to food ingredients can be a key to understand how these organisms regulate and bioprocess many of these food components. Extracts prepared from seven chief functional foods, namely green tea, black tea, Opuntia ficus-indica (prickly pear, cactus pear), black coffee, green coffee, pomegranate, and sumac were administered to a gut consortium culture encompassing 8 microbes which are resembling, to a large extent, the metabolic activities found in the human gut. Samples were harvested at 0.5 and 24 h post addition of functional food extract and from blank culture in parallel and analysed for its metabolites composition using gas chromatography coupled to mass spectrometry detection (GC-MS). A total of 131 metabolites were identified belonging to organic acids, alcohols, amino acids, fatty acids, inorganic compounds, nitrogenous compounds, nucleic acids, phenolics, steroids and sugars, with amino acids as the most abundant class in cultures. Considering the complexity of such datasets, multivariate data analyses were employed to classify samples and investigate how functional foods influence gut microbiota metabolisms. Results from this study provided a first insights regarding how functional foods alter gut metabolism through either induction or inhibition of certain metabolic pathways, i.e. GABA production in the presence of higher acidity induced by functional food metabolites such as polyphenols. Likewise, functional food metabolites i.e., purine alkaloids acted themselves as direct substrate in microbiota metabolism.

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          Most cited references62

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          Formation of propionate and butyrate by the human colonic microbiota

          The human gut microbiota ferments dietary non-digestible carbohydrates into short-chain fatty acids (SCFA). These microbial products are utilized by the host and propionate and butyrate in particular exert a range of health-promoting functions. Here an overview of the metabolic pathways utilized by gut microbes to produce these two SCFA from dietary carbohydrates and from amino acids resulting from protein breakdown is provided. This overview emphasizes the important role played by cross-feeding of intermediary metabolites (in particular lactate, succinate and 1,2-propanediol) between different gut bacteria. The ecophysiology, including growth requirements and responses to environmental factors, of major propionate and butyrate producing bacteria are discussed in relation to dietary modulation of these metabolites. A detailed understanding of SCFA metabolism by the gut microbiota is necessary to underpin effective strategies to optimize SCFA supply to the host.
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            The Brain-Gut-Microbiome Axis

            Preclinical and clinical studies have shown bidirectional interactions within the brain-gut-microbiome axis. Gut microbes communicate to the central nervous system through at least 3 parallel and interacting channels involving nervous, endocrine, and immune signaling mechanisms. The brain can affect the community structure and function of the gut microbiota through the autonomic nervous system, by modulating regional gut motility, intestinal transit and secretion, and gut permeability, and potentially through the luminal secretion of hormones that directly modulate microbial gene expression. A systems biological model is proposed that posits circular communication loops amid the brain, gut, and gut microbiome, and in which perturbation at any level can propagate dysregulation throughout the circuit. A series of largely preclinical observations implicates alterations in brain-gut-microbiome communication in the pathogenesis and pathophysiology of irritable bowel syndrome, obesity, and several psychiatric and neurologic disorders. Continued research holds the promise of identifying novel therapeutic targets and developing treatment strategies to address some of the most debilitating, costly, and poorly understood diseases.
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              Effect of tea phenolics and their aromatic fecal bacterial metabolites on intestinal microbiota.

              Tea is rich in polyphenols and other phenolics that have been widely reported to have beneficial health effects. However, dietary polyphenols are not completely absorbed from the gastrointestinal tract and are metabolized by the gut microflora so that they and their metabolites may accumulate to exert physiological effects. In this study, we investigated the influence of the phenolic components of a tea extract and their aromatic metabolites upon bacterial growth. Fecal homogenates containing bacteria significantly catalyzed tea phenolics, including epicatechin, catechin, 3-O-methyl gallic acid, gallic acid and caffeic acid to generate aromatic metabolites dependent on bacterial species. Different strains of intestinal bacteria had varying degrees of growth sensitivity to tea phenolics and metabolites. Growth of certain pathogenic bacteria such as Clostridium perfringens, Clostridium difficile and Bacteroides spp. was significantly repressed by tea phenolics and their derivatives, while commensal anaerobes like Clostridium spp., Bifidobacterium spp. and probiotics such as Lactobacillus sp. were less severely affected. This indicates that tea phenolics exert significant effects on the intestinal environment by modulation of the intestinal bacterial population, probably by acting as metabolic prebiotics. Our observations provide further evidence for the importance of colonic bacteria in the metabolism, absorption and potential activity of phenolics in human health and disease. The bioactivity of different phenolics may play an important role in the maintenance of gastrointestinal health.
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                Author and article information

                Contributors
                Journal
                J Adv Res
                J Adv Res
                Journal of Advanced Research
                Elsevier
                2090-1232
                2090-1224
                03 January 2020
                May 2020
                03 January 2020
                : 23
                : 47-59
                Affiliations
                [a ]Pharmacognosy Department, College of Pharmacy, Cairo University, Kasr el Aini St., Cairo 11562, Egypt
                [b ]Department of Chemistry, School of Sciences & Engineering, The American University in Cairo, New Cairo 11835, Egypt
                [c ]Pharmacognosy Department, College of Pharmacy, October University for Modern Sciences and Arts (MSA), 6th of October City 12566, Egypt
                [d ]Chemistry Department, Menouffia University, Egypt
                [e ]Helmholtz-Centre for Environmental Research – UFZ GmbH, Department of Molecular Systems Biology, Leipzig, Germany
                [f ]Leibniz Institute of Plant Biochemistry, Department of Bioorganic Chemistry, Weinberg 3, D-06120 Halle (Saale), Germany
                [g ]Institute of Biochemistry, Faculty of Life Sciences, University of Leipzig, Talstraße 33, 04103 Leipzig, Germany
                Author notes
                [* ]Corresponding author at: Pharmacognosy Department, College of Pharmacy, Cairo University, Kasr el Aini St., Cairo 11562, Egypt. mohamed.farag@ 123456pharma.cu.edu.eg
                Article
                S2090-1232(20)30001-1
                10.1016/j.jare.2020.01.001
                7016031
                32071791
                458013eb-3c40-414f-a1e4-8370b5d702b2
                © 2020 Production and hosting by Elsevier B.V. on behalf of Cairo University.

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 28 November 2019
                : 1 January 2020
                : 1 January 2020
                Categories
                Article

                functional foods,gut microbiota,metabolomics,gcms,chemometrics,gc, green coffee,bc, black coffee,gt, green tea,bt, black tea,fi, opuntia ficus-indica (prickly pear),pom, pomegranate (punica granatum),sum, sumac (rhus coriaria),scfas, short chain fatty acids,gi, gastrointestinal,git, gastrointestinal tract

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