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      Dietary cellulose induces anti-inflammatory immunity and transcriptional programs via maturation of the intestinal microbiota

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          ABSTRACT

          Although it is generally accepted that dietary fiber is health promoting, the underlying immunological and molecular mechanisms are not well defined, especially with respect to cellulose, the most ubiquitous dietary fiber. Here, the impact of dietary cellulose on intestinal microbiota, immune responses and gene expression in health and disease was examined. Lack of dietary cellulose disrupted the age-related diversification of the intestinal microbiota, which subsequently remained in an immature state. Interestingly, one of the most affected microbial genera was Alistipes which is equipped with enzymes to degrade cellulose. Absence of cellulose changed the microbial metabolome, skewed intestinal immune responses toward inflammation, altered the gene expression of intestinal epithelial cells and mice showed increased sensitivity to colitis induction. In contrast, mice with a defined microbiota including A. finegoldii showed enhanced colonic expression of intestinal IL-22 and Reg3γ restoring intestinal barrier function. This study supports the epidemiological observations and adds a causal explanation for the health promoting effects of the most common biopolymer on earth.

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          Most cited references66

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          Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies

          16S ribosomal RNA gene (rDNA) amplicon analysis remains the standard approach for the cultivation-independent investigation of microbial diversity. The accuracy of these analyses depends strongly on the choice of primers. The overall coverage and phylum spectrum of 175 primers and 512 primer pairs were evaluated in silico with respect to the SILVA 16S/18S rDNA non-redundant reference dataset (SSURef 108 NR). Based on this evaluation a selection of ‘best available’ primer pairs for Bacteria and Archaea for three amplicon size classes (100–400, 400–1000, ≥1000 bp) is provided. The most promising bacterial primer pair (S-D-Bact-0341-b-S-17/S-D-Bact-0785-a-A-21), with an amplicon size of 464 bp, was experimentally evaluated by comparing the taxonomic distribution of the 16S rDNA amplicons with 16S rDNA fragments from directly sequenced metagenomes. The results of this study may be used as a guideline for selecting primer pairs with the best overall coverage and phylum spectrum for specific applications, therefore reducing the bias in PCR-based microbial diversity studies.
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            Role of the microbiota in immunity and inflammation.

            The microbiota plays a fundamental role on the induction, training, and function of the host immune system. In return, the immune system has largely evolved as a means to maintain the symbiotic relationship of the host with these highly diverse and evolving microbes. When operating optimally, this immune system-microbiota alliance allows the induction of protective responses to pathogens and the maintenance of regulatory pathways involved in the maintenance of tolerance to innocuous antigens. However, in high-income countries, overuse of antibiotics, changes in diet, and elimination of constitutive partners, such as nematodes, may have selected for a microbiota that lack the resilience and diversity required to establish balanced immune responses. This phenomenon is proposed to account for some of the dramatic rise in autoimmune and inflammatory disorders in parts of the world where our symbiotic relationship with the microbiota has been the most affected. Copyright © 2014 Elsevier Inc. All rights reserved.
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              Linking long-term dietary patterns with gut microbial enterotypes.

              Diet strongly affects human health, partly by modulating gut microbiome composition. We used diet inventories and 16S rDNA sequencing to characterize fecal samples from 98 individuals. Fecal communities clustered into enterotypes distinguished primarily by levels of Bacteroides and Prevotella. Enterotypes were strongly associated with long-term diets, particularly protein and animal fat (Bacteroides) versus carbohydrates (Prevotella). A controlled-feeding study of 10 subjects showed that microbiome composition changed detectably within 24 hours of initiating a high-fat/low-fiber or low-fat/high-fiber diet, but that enterotype identity remained stable during the 10-day study. Thus, alternative enterotype states are associated with long-term diet.
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                Author and article information

                Journal
                Gut Microbes
                Gut Microbes
                Gut Microbes
                Taylor & Francis
                1949-0976
                1949-0984
                20 October 2020
                2020
                20 October 2020
                : 12
                : 1
                : 1-17
                Affiliations
                [a ]Institute for Medical Microbiology and Hospital Hygiene, Philipps University; , Marburg, Germany
                [b ]Core Facility for Mass Spectrometry and Elemental Analysis, Philipps University; , Marburg, Germany
                [c ]Institute for Lung Research, Universities of Giessen and Marburg Lung Center, Philipps University; , Marburg, Germany
                [d ]Institute of Anatomy and Cell Biology, Philipps University; , Marburg, Germany
                [e ]Experimental Animal Facility, Biomedical Research Center, Philipps University; , Marburg, Germany
                [f ]Department of Cell Biology and Cell Pathology, Philipps University; , Marburg, Germany
                [g ]Research Unit Analytical BioGeoChemistry, Helmholtz Zentrum München; , Munich, Germany
                [h ]Max Von Pettenkofer-Institute for Hygiene and Clinical Microbiology, Ludwig Maximilians-University München and German Center for Infection Research (DZIF), Partner Site Munich; , Munich, Germany
                [i ]Institute of Laboratory Animal Science, Hannover Medical School; , Hannover, Germany
                [j ]Department Soil Ecology, Helmholtz Centre for Environmental Research - UFZ; , Halle/Saale, Germany
                Author notes
                CONTACT Ulrich Steinhoff ulrich.steinhoff@ 123456staff.uni-marburg.de Institute for Medical Microbiology and Hygiene, University of Marburg, Biomedical Research Center (BMFZ); , Marburg35032, Germany
                Author information
                https://orcid.org/0000-0002-4829-5472
                https://orcid.org/0000-0002-1473-9063
                https://orcid.org/0000-0002-0180-2529
                https://orcid.org/0000-0003-2141-7756
                Article
                1829962
                10.1080/19490976.2020.1829962
                7583510
                33079623
                d68c9121-d248-404a-abfb-f218b06181fe
                © 2020 The Author(s). Published with license by Taylor & Francis Group, LLC.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Figures: 7, References: 70, Pages: 17
                Categories
                Research Article
                Research Paper

                Microbiology & Virology
                cellulose,insoluble fiber,microbiota maturation,microbial diversity,bile acids,mucosal homeostasis,inflammation,alistipes,reg3γ,il-22

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