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      Potential of Pectins to Beneficially Modulate the Gut Microbiota Depends on Their Structural Properties

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          Abstract

          Pectins are plant cell-wall polysaccharides which can be utilized by commensal bacteria in the gut, exhibiting beneficial properties for the host. Knowledge of the impact of pectins on intestinal bacterial communities is insufficient and limited to a few types of pectins. This study characterized the relationship between the structural properties of pectins and their potential to modulate composition and activity of the gut microbiota in a beneficial way. For this purpose we performed in vitro fermentations of nine structurally diverse pectins from citrus fruits and sugar beet, and a pectic derivative, rhamnogalacturonan I (RGI), using a TIM-2 colon model. The composition of microbiota during TIM-2 fermentations was assessed by 16S rRNA gene amplicon sequencing. Both general and pectin-specific changes were observed in relative abundances of numerous bacterial taxa in a time-dependent way. Bacterial populations associated with human health, such as Faecalibacterium prausnitzii, Coprococcus, Ruminococcus, Dorea, Blautia, Oscillospira, Sutterella, Bifidobacterium, Christensenellaceae, Prevotella copri, and Bacteroides spp. were either increased or decreased depending on the substrate, suggesting that these bacteria can be controlled using structurally different pectins. The main structural features linked to the pectin-mediated shifts in microbiota included degree of esterification, composition of neutral sugars, distribution of homogalacturonan and rhamnogalacturonan fractions, degree of branching, and the presence of amide groups. Cumulative production of the total short chain fatty acids and propionate was largest in fermentations of the high methoxyl pectins. Thus, this study indicates that microbial communities in the gut can be specifically modulated by pectins and identifies the features in pectin molecules linked to microbial alterations. This knowledge can be used to define preferred dietary pectins, targeting beneficial bacteria, and favoring more balanced microbiota communities in the gut.

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          Most cited references55

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          QIIME allows analysis of high-throughput community sequencing data.

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            A human gut microbial gene catalogue established by metagenomic sequencing.

            To understand the impact of gut microbes on human health and well-being it is crucial to assess their genetic potential. Here we describe the Illumina-based metagenomic sequencing, assembly and characterization of 3.3 million non-redundant microbial genes, derived from 576.7 gigabases of sequence, from faecal samples of 124 European individuals. The gene set, approximately 150 times larger than the human gene complement, contains an overwhelming majority of the prevalent (more frequent) microbial genes of the cohort and probably includes a large proportion of the prevalent human intestinal microbial genes. The genes are largely shared among individuals of the cohort. Over 99% of the genes are bacterial, indicating that the entire cohort harbours between 1,000 and 1,150 prevalent bacterial species and each individual at least 160 such species, which are also largely shared. We define and describe the minimal gut metagenome and the minimal gut bacterial genome in terms of functions present in all individuals and most bacteria, respectively.
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              The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism.

              Short-chain fatty acids (SCFAs), the end products of fermentation of dietary fibers by the anaerobic intestinal microbiota, have been shown to exert multiple beneficial effects on mammalian energy metabolism. The mechanisms underlying these effects are the subject of intensive research and encompass the complex interplay between diet, gut microbiota, and host energy metabolism. This review summarizes the role of SCFAs in host energy metabolism, starting from the production by the gut microbiota to the uptake by the host and ending with the effects on host metabolism. There are interesting leads on the underlying molecular mechanisms, but there are also many apparently contradictory results. A coherent understanding of the multilevel network in which SCFAs exert their effects is hampered by the lack of quantitative data on actual fluxes of SCFAs and metabolic processes regulated by SCFAs. In this review we address questions that, when answered, will bring us a great step forward in elucidating the role of SCFAs in mammalian energy metabolism.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                15 February 2019
                2019
                : 10
                : 223
                Affiliations
                [1] 1Department of Food Science, University of Copenhagen , Copenhagen, Denmark
                [2] 2Center for Healthy Eating and Food Innovation, Maastricht University – Campus Venlo , Maastricht, Netherlands
                [3] 3Department of Environmental Science, Aarhus University , Roskilde, Denmark
                [4] 4CP Kelco ApS , Lille Skensved, Denmark
                [5] 5Department of Plant and Environmental Sciences, University of Copenhagen , Copenhagen, Denmark
                [6] 6Beneficial Microbes Consultancy , Wageningen, Netherlands
                Author notes

                Edited by: Vittorio Capozzi, University of Foggia, Italy

                Reviewed by: Lorena Ruiz, Instituto de Productos Lácteos de Asturias (IPLA), Spain; Stefano Campanaro, University of Padua, Italy

                *Correspondence: Nadja Larsen, nf@ 123456food.ku.dk

                This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2019.00223
                6384267
                30828323
                fefb5d4a-046d-48b5-a168-6d1b3af7cc9f
                Copyright © 2019 Larsen, Bussolo de Souza, Krych, Barbosa Cahú, Wiese, Kot, Hansen, Blennow, Venema and Jespersen.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 07 December 2018
                : 28 January 2019
                Page count
                Figures: 5, Tables: 3, Equations: 0, References: 56, Pages: 13, Words: 0
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                gut microbiota,pectins,structure-function relationship,tim-2 colon model,short-chain fatty acids

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