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      Microbial imbalance in inflammatory bowel disease patients at different taxonomic levels

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          Abstract

          Background

          Inflammatory bowel disease (IBD), is a debilitating group of chronic diseases including Crohn’s Disease (CD) and ulcerative colitis (UC), which causes inflammation of the gut and affects millions of people worldwide. At different taxonomic levels, the structure of the gut microbiota is significantly altered in IBD patients compared to that of healthy individuals. However, it is unclear how these IBD-affected bacterial groups are related to other common bacteria in the gut, and how they are connected across different disease conditions at the global scale.

          Results

          In this study, using faecal samples from patients with IBD, we show through diversity analysis of the microbial community structure based on the 16S rRNA gene that the gut microbiome of IBD patients is less diverse compared to healthy individuals. Furthermore, we have identified which bacterial groups change in abundance in both CD and UC compared to healthy controls. A substantial imbalance was observed across four major bacterial phyla including Firmicutes, Bacteroidetes, Proteobacteria and Actinobacteria, which together constitute > 98% of the gut microbiota. Next, we reconstructed a bacterial family co-abundance network based on the correlation of abundance profiles obtained from the public gut microbiome data of > 22,000 samples of faecal and gut biopsies taken from both diseased and healthy individuals. The data was compiled using the EBI metagenomics database (Mitchell et al. in Nucleic Acids Res 46:D726–D735, 2018). By mapping IBD-altered bacterial families to the network, we show that the bacterial families which exhibit an increased abundance in IBD conditions are not well connected to other groups, implying that these families generally do not coexist together with common gut organisms. Whereas, the bacterial families whose abundance is reduced or did not change in IBD conditions compared to healthy conditions are very well connected to other bacterial groups, suggesting they are highly important groups of bacteria in the gut that can coexist with other bacteria across a range of conditions.

          Conclusions

          IBD patients exhibited a less diverse gut microbiome compared to healthy individuals. Bacterial groups which changed in IBD patients were found to be groups which do not co-exist well with common commensal gut bacteria, whereas bacterial groups which did not change in patients with IBD were found to commonly co-exist with commensal gut microbiota. This gives a potential insight into the dynamics of the gut microbiota in patients with IBD.

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          Most cited references34

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          DADA2: High resolution sample inference from Illumina amplicon data

          We present DADA2, a software package that models and corrects Illumina-sequenced amplicon errors. DADA2 infers sample sequences exactly, without coarse-graining into OTUs, and resolves differences of as little as one nucleotide. In several mock communities DADA2 identified more real variants and output fewer spurious sequences than other methods. We applied DADA2 to vaginal samples from a cohort of pregnant women, revealing a diversity of previously undetected Lactobacillus crispatus variants.
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            phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data

            Background The analysis of microbial communities through DNA sequencing brings many challenges: the integration of different types of data with methods from ecology, genetics, phylogenetics, multivariate statistics, visualization and testing. With the increased breadth of experimental designs now being pursued, project-specific statistical analyses are often needed, and these analyses are often difficult (or impossible) for peer researchers to independently reproduce. The vast majority of the requisite tools for performing these analyses reproducibly are already implemented in R and its extensions (packages), but with limited support for high throughput microbiome census data. Results Here we describe a software project, phyloseq, dedicated to the object-oriented representation and analysis of microbiome census data in R. It supports importing data from a variety of common formats, as well as many analysis techniques. These include calibration, filtering, subsetting, agglomeration, multi-table comparisons, diversity analysis, parallelized Fast UniFrac, ordination methods, and production of publication-quality graphics; all in a manner that is easy to document, share, and modify. We show how to apply functions from other R packages to phyloseq-represented data, illustrating the availability of a large number of open source analysis techniques. We discuss the use of phyloseq with tools for reproducible research, a practice common in other fields but still rare in the analysis of highly parallel microbiome census data. We have made available all of the materials necessary to completely reproduce the analysis and figures included in this article, an example of best practices for reproducible research. Conclusions The phyloseq project for R is a new open-source software package, freely available on the web from both GitHub and Bioconductor.
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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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                Author and article information

                Contributors
                T.Alam@warwick.ac.uk
                E.M.H.Wellington@warwick.ac.uk
                Journal
                Gut Pathog
                Gut Pathog
                Gut Pathogens
                BioMed Central (London )
                1757-4749
                4 January 2020
                4 January 2020
                2020
                : 12
                : 1
                Affiliations
                [1 ]ISNI 0000 0000 8809 1613, GRID grid.7372.1, Warwick Medical School, , University of Warwick, ; Coventry, UK
                [2 ]ISNI 0000 0000 8809 1613, GRID grid.7372.1, School of Life Sciences, , University of Warwick, ; Coventry, UK
                [3 ]GRID grid.15628.38, Department of Gastroenterology, , University Hospitals Coventry & Warwickshire NHS Trust, ; Clifford Bridge Road, Coventry, CV2 2DX UK
                [4 ]ISNI 0000000106754565, GRID grid.8096.7, School of Life Sciences, , University of Coventry, ; Coventry, UK
                [5 ]ISNI 0000 0004 1936 8411, GRID grid.9918.9, Faculty of Life Science, , University of Leicester, ; Leicester, UK
                [6 ]ISNI 0000 0001 2199 6511, GRID grid.70909.37, Present Address: G.C.A.A National Institute for Biological Standards and Control (NIBSC), ; Potters Bar, UK
                Author information
                http://orcid.org/0000-0002-6872-0691
                Article
                341
                10.1186/s13099-019-0341-6
                6942256
                31911822
                b0b8e585-1b1e-4470-9e37-7e0395574959
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 19 September 2019
                : 12 December 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BBSRC BB/L027801/1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100004443, Warwick Medical School;
                Funded by: FAPIC
                Award ID: SEP-210176939 2015-2020
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                Gastroenterology & Hepatology
                inflammatory bowel disease,crohn’s disease,ulcerative colitis,gut microbiota,microbial imbalance

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