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      Environmental and Gut Bacteroidetes: The Food Connection

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          Abstract

          Members of the diverse bacterial phylum Bacteroidetes have colonized virtually all types of habitats on Earth. They are among the major members of the microbiota of animals, especially in the gastrointestinal tract, can act as pathogens and are frequently found in soils, oceans and freshwater. In these contrasting ecological niches, Bacteroidetes are increasingly regarded as specialists for the degradation of high molecular weight organic matter, i.e., proteins and carbohydrates. This review presents the current knowledge on the role and mechanisms of polysaccharide degradation by Bacteroidetes in their respective habitats. The recent sequencing of Bacteroidetes genomes confirms the presence of numerous carbohydrate-active enzymes covering a large spectrum of substrates from plant, algal, and animal origin. Comparative genomics reveal specific Polysaccharide Utilization Loci shared between distantly related members of the phylum, either in environmental or gut-associated species. Moreover, Bacteroidetes genomes appear to be highly plastic and frequently reorganized through genetic rearrangements, gene duplications and lateral gene transfers (LGT), a feature that could have driven their adaptation to distinct ecological niches. Evidence is accumulating that the nature of the diet shapes the composition of the intestinal microbiota. We address the potential links between gut and environmental bacteria through food consumption. LGT can provide gut bacteria with original sets of utensils to degrade otherwise refractory substrates found in the diet. A more complete understanding of the genetic gateways between food-associated environmental species and intestinal microbial communities sheds new light on the origin and evolution of Bacteroidetes as animals’ symbionts. It also raises the question as to how the consumption of increasingly hygienic and processed food deprives our microbiota from useful environmental genes and possibly affects our health.

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          Most cited references134

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          A microbial symbiosis factor prevents intestinal inflammatory disease.

          Humans are colonized by multitudes of commensal organisms representing members of five of the six kingdoms of life; however, our gastrointestinal tract provides residence to both beneficial and potentially pathogenic microorganisms. Imbalances in the composition of the bacterial microbiota, known as dysbiosis, are postulated to be a major factor in human disorders such as inflammatory bowel disease. We report here that the prominent human symbiont Bacteroides fragilis protects animals from experimental colitis induced by Helicobacter hepaticus, a commensal bacterium with pathogenic potential. This beneficial activity requires a single microbial molecule (polysaccharide A, PSA). In animals harbouring B. fragilis not expressing PSA, H. hepaticus colonization leads to disease and pro-inflammatory cytokine production in colonic tissues. Purified PSA administered to animals is required to suppress pro-inflammatory interleukin-17 production by intestinal immune cells and also inhibits in vitro reactions in cell cultures. Furthermore, PSA protects from inflammatory disease through a functional requirement for interleukin-10-producing CD4+ T cells. These results show that molecules of the bacterial microbiota can mediate the critical balance between health and disease. Harnessing the immunomodulatory capacity of symbiosis factors such as PSA might potentially provide therapeutics for human inflammatory disorders on the basis of entirely novel biological principles.
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            How host-microbial interactions shape the nutrient environment of the mammalian intestine.

            Humans and other mammals are colonized by a vast, complex, and dynamic consortium of microorganisms. One evolutionary driving force for maintaining this metabolically active microbial society is to salvage energy from nutrients, particularly carbohydrates, that are otherwise nondigestible by the host. Much of our understanding of the molecular mechanisms by which members of the intestinal microbiota degrade complex polysaccharides comes from studies of Bacteroides thetaiotaomicron, a prominent and genetically manipulatable component of the normal human and mouse gut. Colonization of germ-free mice with B. thetaiotaomicron has shown how this anaerobe modifies many aspects of intestinal cellular differentiation/gene expression to benefit both host and microbe. These and other studies underscore the importance of understanding precisely how nutrient metabolism serves to establish and sustain symbiotic relationships between mammals and their bacterial partners.
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              Comparative Analysis of Human Gut Microbiota by Barcoded Pyrosequencing

              Humans host complex microbial communities believed to contribute to health maintenance and, when in imbalance, to the development of diseases. Determining the microbial composition in patients and healthy controls may thus provide novel therapeutic targets. For this purpose, high-throughput, cost-effective methods for microbiota characterization are needed. We have employed 454-pyrosequencing of a hyper-variable region of the 16S rRNA gene in combination with sample-specific barcode sequences which enables parallel in-depth analysis of hundreds of samples with limited sample processing. In silico modeling demonstrated that the method correctly describes microbial communities down to phylotypes below the genus level. Here we applied the technique to analyze microbial communities in throat, stomach and fecal samples. Our results demonstrate the applicability of barcoded pyrosequencing as a high-throughput method for comparative microbial ecology.
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                Author and article information

                Journal
                Front Microbiol
                Front. Microbio.
                Frontiers in Microbiology
                Frontiers Research Foundation
                1664-302X
                30 May 2011
                2011
                : 2
                : 93
                Affiliations
                [1] 1simpleUMR 7139, Marine Plants and Biomolecules, Station Biologique de Roscoff, UPMC University Paris 6, Roscoff, France
                [2] 2simpleUMR 7139, Marine Plants and Biomolecules, Station Biologique de Roscoff CNRS, Roscoff, France
                Author notes

                Edited by: Peter J. Turnbaugh, Harvard University, USA

                Reviewed by: Deborah Threadgill, North Carolina State University, USA; Alain Stintzi, Ottawa Institute of Systems Biology, Canada

                *Correspondence: Gurvan Michel, UMR 7139, CNRS/UPMC, Marine Plants and Biomolecules, Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France. e-mail: gurvan@ 123456sb-roscoff.fr

                Current address: Jan-Hendrik Hehemann, Department of Biochemistry and Microbiology, University of Victoria, PO Box 3055 STN CSC, Victoria, BC, Canada V8W 3PG;

                Etienne Rebuffet, Department of Chemistry, Biochemistry and Biophysics, University of Gothenburg, Box 462, SE-405 30 Göteborg, Sweden.

                This article was submitted to Frontiers in Cellular and Infection Microbiology, a specialty of Frontiers in Microbiology.

                Article
                10.3389/fmicb.2011.00093
                3129010
                21747801
                206536c1-d8eb-43a1-aabd-64d97366d52c
                Copyright © 2011 Thomas, Hehemann, Rebuffet, Czjzek and Michel.

                This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.

                History
                : 12 January 2011
                : 14 April 2011
                Page count
                Figures: 2, Tables: 2, Equations: 0, References: 210, Pages: 16, Words: 16457
                Categories
                Microbiology
                Review Article

                Microbiology & Virology
                adaptation to environmental niches,bacteroidetes,microbiota
                Microbiology & Virology
                adaptation to environmental niches, bacteroidetes, microbiota

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