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      Asymptomatic Intestinal Colonization with Protist Blastocystis Is Strongly Associated with Distinct Microbiome Ecological Patterns

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          Abstract

          Given the results of our study and other reports of the effects of the most common human gut protist on the diversity and composition of the bacterial microbiome, Blastocystis and, possibly, other gut protists should be studied as ecosystem engineers that drive community diversity and composition.

          ABSTRACT

          Blastocystis is the most prevalent protist of the human intestine, colonizing approximately 20% of the North American population and up to 100% in some nonindustrialized settings. Blastocystis is associated with gastrointestinal and systemic disease but can also be an asymptomatic colonizer in large populations. While recent findings in humans have shown bacterial microbiota changes associated with this protist, it is unknown whether these occur due to the presence of Blastocystis or as a result of inflammation. To explore this, we evaluated the fecal bacterial and eukaryotic microbiota in 156 asymptomatic adult subjects from a rural population in Xoxocotla, Mexico. Colonization with Blastocystis was strongly associated with an increase in bacterial alpha diversity and broad changes in beta diversity and with more discrete changes to the microbial eukaryome. More than 230 operational taxonomic units (OTUs), including those of dominant species Prevotella copri and Ruminococcus bromii, were differentially abundant in Blastocystis-colonized individuals. Large functional changes accompanied these observations, with differential abundances of 202 (out of 266) predicted metabolic pathways (PICRUSt), as well as lower fecal concentrations of acetate, butyrate, and propionate in colonized individuals. Fecal calprotectin was markedly decreased in association with Blastocystis colonization, suggesting that this ecological shift induces subclinical immune consequences to the asymptomatic host. This work is the first to show a direct association between the presence of Blastocystis and shifts in the gut bacterial and eukaryotic microbiome in the absence of gastrointestinal disease or inflammation. These results prompt further investigation of the role Blastocystis and other eukaryotes play within the human microbiome.

          IMPORTANCE Given the results of our study and other reports of the effects of the most common human gut protist on the diversity and composition of the bacterial microbiome, Blastocystis and, possibly, other gut protists should be studied as ecosystem engineers that drive community diversity and composition.

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          Most cited references57

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          Oligotyping: differentiating between closely related microbial taxa using 16S rRNA gene data

          Bacteria comprise the most diverse domain of life on Earth, where they occupy nearly every possible ecological niche and play key roles in biological and chemical processes. Studying the composition and ecology of bacterial ecosystems and understanding their function are of prime importance. High-throughput sequencing technologies enable nearly comprehensive descriptions of bacterial diversity through 16S ribosomal RNA gene amplicons. Analyses of these communities generally rely upon taxonomic assignments through reference data bases or clustering approaches using de facto sequence similarity thresholds to identify operational taxonomic units. However, these methods often fail to resolve ecologically meaningful differences between closely related organisms in complex microbial data sets. In this paper, we describe oligotyping, a novel supervised computational method that allows researchers to investigate the diversity of closely related but distinct bacterial organisms in final operational taxonomic units identified in environmental data sets through 16S ribosomal RNA gene data by the canonical approaches. Our analysis of two data sets from two different environments demonstrates the capacity of oligotyping at discriminating distinct microbial populations of ecological importance. Oligotyping can resolve the distribution of closely related organisms across environments and unveil previously overlooked ecological patterns for microbial communities. The URL http://oligotyping.org offers an open-source software pipeline for oligotyping.
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            New insights on classification, identification, and clinical relevance of Blastocystis spp.

            Blastocystis is an unusual enteric protozoan parasite of humans and many animals. It has a worldwide distribution and is often the most commonly isolated organism in parasitological surveys. The parasite has been described since the early 1900s, but only in the last decade or so have there been significant advances in our understanding of Blastocystis biology. However, the pleomorphic nature of the parasite and the lack of standardization in techniques have led to confusion and, in some cases, misinterpretation of data. This has hindered laboratory diagnosis and efforts to understand its mode of reproduction, life cycle, prevalence, and pathogenesis. Accumulating epidemiological, in vivo, and in vitro data strongly suggest that Blastocystis is a pathogen. Many genotypes exist in nature, and recent observations indicate that humans are, in reality, hosts to numerous zoonotic genotypes. Such genetic diversity has led to a suggestion that previously conflicting observations on the pathogenesis of Blastocystis are due to pathogenic and nonpathogenic genotypes. Recent epidemiological, animal infection, and in vitro host-Blastocystis interaction studies suggest that this may indeed be the case. This review focuses on such recent advances and also provides updates on laboratory and clinical aspects of Blastocystis spp.
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              Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut.

              The mechanism to maintain homeostasis of the gut microbiota remains largely unknown despite its critical role in the body defense. In the intestines of mice with deficiency of activation-induced cytidine deaminase (AID), the absence of hypermutated IgA is partially compensated for by the presence of large amounts of unmutated IgM and normal expression levels of defensins and angiogenins. We show here a predominant and persistent expansion of segmented filamentous bacteria throughout the small intestine of AID(-/-) mice. Reconstitution of lamina propria IgA production in AID(-/-) mice recovered the normal composition of gut flora and abolished the local and systemic activation of the immune system. The results indicate that secretions of IgAs rather than innate defense peptides are critical to regulation of commensal bacterial flora and that the segmented filamentous bacteria antigens are strong stimuli of the mucosal immune system.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                mSystems
                mSystems
                msys
                msys
                mSystems
                mSystems
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5077
                26 June 2018
                May-Jun 2018
                : 3
                : 3
                : e00007-18
                Affiliations
                [a ]Laboratorio de Inmunología del Departamento de Medicina Experimental, UNAM, Mexico City, Mexico
                [b ]Michael Smith Laboratories, Department of Microbiology & Immunology, University of British Columbia, Vancouver, British Columbia, Canada
                [c ]Department of Physiology & Pharmacology, University of Calgary, Calgary, Alberta, Canada
                [d ]Department of Pediatrics, University of Calgary, Calgary, Alberta, Canada
                [e ]Department of Biochemistry and Microbiology, University of Victoria, Victoria, British Columbia, Canada
                [f ]Department of Zoology, University of British Columbia, Vancouver, British Columbia, Canada
                [g ]Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada
                [h ]Department of Agricultural, Food and Nutritional Sciences, University of Alberta, Edmonton, Alberta, Canada
                [i ]School of Life Sciences, Northwestern Polytechnical University, Xi’an, China
                [j ]Unidad de Investigación en Enfermedades Infecciosas, UMAE Pediatria, IMSS, Mexico City, Mexico
                [k ]Department of Biochemistry and Molecular Biology, University of British Columbia, Vancouver, British Columbia, Canada
                University of Colorado Denver
                Author notes
                Address correspondence to M. C. Arrieta, marie.arrieta@ 123456ucalgary.ca , or C. Ximénez-García, cximenez@ 123456unam.mx , or B. B. Finlay, bfinlay@ 123456msl.ubc.ca .

                M.C.A., C.X.-G., and B.B.F. share equal senior authorship.

                Citation Nieves-Ramírez ME, Partida-Rodríguez O, Laforest-Lapointe I, Reynolds LA, Brown EM, Valdez-Salazar A, Morán-Silva P, Rojas-Velázquez L, Morien E, Parfrey LW, Jin M, Walter J, Torres J, Arrieta MC, Ximénez-García C, Finlay BB. 2018. Asymptomatic intestinal colonization with protist Blastocystis is strongly associated with distinct microbiome ecological patterns. mSystems 3:e00007-18. https://doi.org/10.1128/mSystems.00007-18.

                Author information
                https://orcid.org/0000-0002-4490-3370
                Article
                mSystems00007-18
                10.1128/mSystems.00007-18
                6020473
                29963639
                a3f272c8-b72e-4ba5-a431-2e3337d7f845
                Copyright © 2018 Nieves-Ramírez et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 23 January 2018
                : 2 May 2018
                Page count
                supplementary-material: 10, Figures: 5, Tables: 1, Equations: 0, References: 98, Pages: 18, Words: 12090
                Funding
                Funded by: PAPIIT UNAM;
                Award ID: IN218214
                Award Recipient :
                Funded by: IMSS;
                Award ID: FIS/IMSS/PROT/1368
                Award Recipient :
                Funded by: Human Frontier Science Program (HFSP), https://doi.org/10.13039/501100000854;
                Award ID: RGY0078/2015
                Award Recipient :
                Funded by: Consejo Nacional de Ciencia y Tecnología (CONACYT), https://doi.org/10.13039/501100003141;
                Award ID: 272601
                Award ID: 283522
                Award ID: 257091
                Award Recipient : Award Recipient :
                Funded by: Consejo Nacional de Ciencia y Tecnología (CONACYT), https://doi.org/10.13039/501100003141;
                Award ID: 235618
                Award ID: 208253
                Award Recipient : Award Recipient :
                Funded by: Gouvernement du Canada | Canadian Institutes of Health Research (CIHR), https://doi.org/10.13039/501100000024;
                Award ID: FRN148484
                Award ID: FRN148547
                Award Recipient :
                Categories
                Research Article
                Host-Microbe Biology
                Custom metadata
                May/June 2018

                blastocystis,gut microbiome,eukaryome,host-microbe interactions,microbial ecology

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