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      A Fungal World: Could the Gut Mycobiome Be Involved in Neurological Disease?

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          Abstract

          The human microbiome has received decades of attention from scientific and medical research communities. The human gastrointestinal tract is host to immense populations of microorganisms including bacteria, viruses, archaea, and fungi (the gut microbiota). High-throughput sequencing and computational advancements provide unprecedented ability to investigate the structure and function of microbial communities associated with the human body in health and disease. Most research to date has largely focused on elucidating the bacterial component of the human gut microbiota. Study of the gut “mycobiota,” which refers to the diverse array of fungal species, is a relatively new and rapidly progressing field. Though omnipresent, the number and abundance of fungi occupying the human gut is orders of magnitude smaller than that of bacteria. Recent insights however, have suggested that the gut mycobiota may be intricately linked to health and disease. Evaluation of the gut mycobiota has shown that not only are the fungal communities altered in disease, but they also play a role in maintaining intestinal homeostasis and influencing systemic immunity. In addition, it is now widely accepted that host-fungi and bacteria-fungi associations are critical to host health. While research of the gut mycobiota in health and disease is on the rise, little research has been performed in the context of neuroimmune and neurodegenerative conditions. Gut microbiota dysbiosis (specifically bacteria and archaea) have been reported in neurological diseases such as multiple sclerosis, amyotrophic lateral sclerosis, and Alzheimer's, among others. Given the widely accepted bacteria-fungi associations and paucity of mycobiota-specific studies in neurological disease, this review discusses the potential role fungi may play in multiple sclerosis and other neurological diseases. Herein, we provide an overview of recent advances in gut mycobiome research and discuss the plausible role of both intestinal and non-intestinal fungi in the context of neuroimmune and neurodegenerative conditions.

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          Most cited references75

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          The gut microbiome in health and in disease

          Recent technological advancements and expanded efforts have led to a tremendous growth in the collective knowledge of the human microbiome. This review will highlight some of the important recent findings in this area of research.
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            Fungal microbiota dysbiosis in IBD

            Objective The bacterial intestinal microbiota plays major roles in human physiology and IBDs. Although some data suggest a role of the fungal microbiota in IBD pathogenesis, the available data are scarce. The aim of our study was to characterise the faecal fungal microbiota in patients with IBD. Design Bacterial and fungal composition of the faecal microbiota of 235 patients with IBD and 38 healthy subjects (HS) was determined using 16S and ITS2 sequencing, respectively. The obtained sequences were analysed using the Qiime pipeline to assess composition and diversity. Bacterial and fungal taxa associated with clinical parameters were identified using multivariate association with linear models. Correlation between bacterial and fungal microbiota was investigated using Spearman's test and distance correlation. Results We observed that fungal microbiota is skewed in IBD, with an increased Basidiomycota/Ascomycota ratio, a decreased proportion of Saccharomyces cerevisiae and an increased proportion of Candida albicans compared with HS. We also identified disease-specific alterations in diversity, indicating that a Crohn's disease-specific gut environment may favour fungi at the expense of bacteria. The concomitant analysis of bacterial and fungal microbiota showed a dense and homogenous correlation network in HS but a dramatically unbalanced network in IBD, suggesting the existence of disease-specific inter-kingdom alterations. Conclusions Besides bacterial dysbiosis, our study identifies a distinct fungal microbiota dysbiosis in IBD characterised by alterations in biodiversity and composition. Moreover, we unravel here disease-specific inter-kingdom network alterations in IBD, suggesting that, beyond bacteria, fungi might also play a role in IBD pathogenesis.
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              Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis.

              The intestinal microflora, typically equated with bacteria, influences diseases such as obesity and inflammatory bowel disease. Here, we show that the mammalian gut contains a rich fungal community that interacts with the immune system through the innate immune receptor Dectin-1. Mice lacking Dectin-1 exhibited increased susceptibility to chemically induced colitis, which was the result of altered responses to indigenous fungi. In humans, we identified a polymorphism in the gene for Dectin-1 (CLEC7A) that is strongly linked to a severe form of ulcerative colitis. Together, our findings reveal a eukaryotic fungal community in the gut (the "mycobiome") that coexists with bacteria and substantially expands the repertoire of organisms interacting with the intestinal immune system to influence health and disease.
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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
                09 January 2019
                2018
                : 9
                : 3249
                Affiliations
                [1] 1Department of Internal Medicine, University of Manitoba , Winnipeg, MB, Canada
                [2] 2IBD Clinical and Research Centre, University of Manitoba , Winnipeg, MB, Canada
                [3] 3National Microbiology Laboratory, Public Health Agency of Canada , Winnipeg, MB, Canada
                [4] 4Centre for Brain Health and Faculty of Medicine (Neurology), University of British Columbia , Vancouver, BC, Canada
                [5] 5Department of Medical Microbiology and Infectious Diseases, University of Manitoba , Winnipeg, MB, Canada
                Author notes

                Edited by: Esteban A. Hernandez-Vargas, Frankfurt Institute for Advanced Studies, Germany

                Reviewed by: Irun R. Cohen, Weizmann Institute of Science, Israel; Allison B. Reiss, Winthrop University Hospital, United States

                *Correspondence: Natalie C. Knox natalie.knox@ 123456canada.ca

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

                †Present Address: Jessica D. Forbes, Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, Canada

                Article
                10.3389/fmicb.2018.03249
                6333682
                30687254
                61621427-bb8e-44e2-b2b8-a1bdf2dad1cc
                Copyright © 2019 Forbes, Bernstein, Tremlett, Van Domselaar and Knox.

                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
                : 28 September 2018
                : 14 December 2018
                Page count
                Figures: 2, Tables: 1, Equations: 0, References: 106, Pages: 13, Words: 10849
                Categories
                Microbiology
                Review

                Microbiology & Virology
                gut,mycobiome,mycobiota,fungi,neurological disease,multiple sclerosis
                Microbiology & Virology
                gut, mycobiome, mycobiota, fungi, neurological disease, multiple sclerosis

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