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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 references 16

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          Inflammatory bowel disease.

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            Metabolic dependencies drive species co-occurrence in diverse microbial communities.

            Microbial communities populate most environments on earth and play a critical role in ecology and human health. Their composition is thought to be largely shaped by interspecies competition for the available resources, but cooperative interactions, such as metabolite exchanges, have also been implicated in community assembly. The prevalence of metabolic interactions in microbial communities, however, has remained largely unknown. Here, we systematically survey, by using a genome-scale metabolic modeling approach, the extent of resource competition and metabolic exchanges in over 800 communities. We find that, despite marked resource competition at the level of whole assemblies, microbial communities harbor metabolically interdependent groups that recur across diverse habitats. By enumerating flux-balanced metabolic exchanges in these co-occurring subcommunities we also predict the likely exchanged metabolites, such as amino acids and sugars, that can promote group survival under nutritionally challenging conditions. Our results highlight metabolic dependencies as a major driver of species co-occurrence and hint at cooperative groups as recurring modules of microbial community architecture.
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              Differences between tissue-associated intestinal microfloras of patients with Crohn's disease and ulcerative colitis.

              A leading hypothesis for the role of bacteria in inflammatory bowel diseases is that an imbalance in normal gut flora is a prerequisite for inflammation. Testing this hypothesis requires comparisons between the microbiota compositions of ulcerative colitis and Crohn's disease patients and those of healthy individuals. In this study, we obtained biopsy samples from patients with Crohn's disease and ulcerative colitis and from healthy controls. Bacterial DNA was extracted from the tissue samples, amplified using universal bacterial 16S rRNA gene primers, and cloned into a plasmid vector. Insert-containing colonies were picked for high-throughput sequencing, and sequence data were analyzed, yielding species-level phylogenetic data. The clone libraries yielded 3,305 sequenced clones, representing 151 operational taxonomical units. There was no significant difference between floras from inflamed and healthy tissues from within the same individual. Proteobacteria were significantly (P = 0.0007) increased in Crohn's disease patients, as were Bacteroidetes (P < 0.0001), while Clostridia were decreased in that group (P < 0.0001) in comparison with the healthy and ulcerative colitis groups, which displayed no significant differences. Thus, the bacterial flora composition of Crohn's patients appears to be significantly altered from that of healthy controls, unlike that of ulcerative colitis patients. Imbalance in flora in Crohn's disease is probably not sufficient to cause inflammation, since microbiotas from inflamed and noninflamed tissues were of similar compositions within the same individual.
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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
                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
                Article
                341
                10.1186/s13099-019-0341-6
                6942256
                © 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.

                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

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