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      Shifting the paradigm from pathogens to pathobiome: new concepts in the light of meta-omics

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          Abstract

          The concept of pathogenesis has evolved considerably over recent years, and the scenario “a microbe + virulence factors = disease” is probably far from reality in a number of cases. Actual pathogens have extremely broad biological diversity and are found in all major groups of microorganisms (viruses, bacteria, fungi, protozoa…). Their pathogenicity results from strong and often highly specific interactions they have with either their microbial environment, hosts and/or arthropod vectors. In this review, we explore the contribution of metagenomic approaches toward understanding pathogens within the context of microbial communities. With this broader view, we discussed the concept of “pathobiome” and the research questions that this raises.

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          Most cited references45

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          454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity.

          * Soil fungi play a major role in ecological and biogeochemical processes in forests. Little is known, however, about the structure and richness of different fungal communities and the distribution of functional ecological groups (pathogens, saprobes and symbionts). * Here, we assessed the fungal diversity in six different forest soils using tag-encoded 454 pyrosequencing of the nuclear ribosomal internal transcribed spacer-1 (ITS-1). No less than 166 350 ITS reads were obtained from all samples. In each forest soil sample (4 g), approximately 30 000 reads were recovered, corresponding to around 1000 molecular operational taxonomic units. * Most operational taxonomic units (81%) belonged to the Dikarya subkingdom (Ascomycota and Basidiomycota). Richness, abundance and taxonomic analyses identified the Agaricomycetes as the dominant fungal class. The ITS-1 sequences (73%) analysed corresponded to only 26 taxa. The most abundant operational taxonomic units showed the highest sequence similarity to Ceratobasidium sp., Cryptococcus podzolicus, Lactarius sp. and Scleroderma sp. * This study validates the effectiveness of high-throughput 454 sequencing technology for the survey of soil fungal diversity. The large proportion of unidentified sequences, however, calls for curated sequence databases. The use of pyrosequencing on soil samples will accelerate the study of the spatiotemporal dynamics of fungal communities in forest ecosystems.
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            Intestinal microbiota promote enteric virus replication and systemic pathogenesis.

            Intestinal bacteria aid host health and limit bacterial pathogen colonization. However, the influence of bacteria on enteric viruses is largely unknown. We depleted the intestinal microbiota of mice with antibiotics before inoculation with poliovirus, an enteric virus. Antibiotic-treated mice were less susceptible to poliovirus disease and supported minimal viral replication in the intestine. Exposure to bacteria or their N-acetylglucosamine-containing surface polysaccharides, including lipopolysaccharide and peptidoglycan, enhanced poliovirus infectivity. We found that poliovirus binds lipopolysaccharide, and exposure of poliovirus to bacteria enhanced host cell association and infection. The pathogenesis of reovirus, an unrelated enteric virus, also was more severe in the presence of intestinal microbes. These results suggest that antibiotic-mediated microbiota depletion diminishes enteric virus infection and that enteric viruses exploit intestinal microbes for replication and transmission.
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              A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance.

              A mutualistic association between a fungal endophyte and a tropical panic grass allows both organisms to grow at high soil temperatures. We characterized a virus from this fungus that is involved in the mutualistic interaction. Fungal isolates cured of the virus are unable to confer heat tolerance, but heat tolerance is restored after the virus is reintroduced. The virus-infected fungus confers heat tolerance not only to its native monocot host but also to a eudicot host, which suggests that the underlying mechanism involves pathways conserved between these two groups of plants.
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                Author and article information

                Journal
                Front Cell Infect Microbiol
                Front Cell Infect Microbiol
                Front. Cell. Infect. Microbiol.
                Frontiers in Cellular and Infection Microbiology
                Frontiers Media S.A.
                2235-2988
                05 March 2014
                2014
                : 4
                : 29
                Affiliations
                [1] 1INRA, UMR BIPAR (Enva/Anses) USC INRA Maisons-Alfort, France
                [2] 2CIRAD, UMR CMAEE Petit-Bourg, Guadeloupe, France
                [3] 3INRA, UMR 1309 CMAEE Montpellier, France
                [4] 4INRA, Université de Toulouse, INP, ENVT, UMR 1225, IHAP Toulouse, France
                [5] 5INRA, UMR CBGP (INRA/IRD/Cirad/Montpellier SupAgro) Montferrier-sur-Lez, France
                [6] 6INRA, Institut de Recherche en Horticulture et Semences, UMR 1345 Angers, France
                [7] 7INRA, UMR 1290, BIOGER-CPP, INRA AgroParis Tech Thiverval-Grignon, France
                [8] 8INRA, UMR 1253 STLO Rennes, France
                [9] 9Agrocampus Ouest, UMR 1253 STLO Rennes, France
                [10] 10INRA, UMR 1333 DGIMI Montpellier, France
                [11] 11INRA, UMR 1319, Micalis Jouy-en-Josas, France
                [12] 12CIRAD/UMR BGPI TA A54/K Montpellier Cedex 5, France
                [13] 13UMR 1332 Biologie du Fruit et Pathologie, INRA Villenave d'Ornon Cedex, France
                [14] 14UMR 1332 Biologie du Fruit et Pathologie, Université de Bordeaux Villenave d'Ornon Cedex, France
                Author notes

                Edited by: Patrick Mavingui, Centre National de la Recherche Scientifique, France

                Reviewed by: Valerio Iebba, 'Sapienza' University of Rome, Italy; Catherine Legras-Lachuer, Université Lyon1, France

                *Correspondence: Muriel Vayssier-Taussat, Institut National de la Recherche Agronomique, Animal Health, USC Bartonella et Tiques, 23 Avenue du Général de Gaulle, 94 700 Maisons-Alfort, France e-mail: mvayssier@ 123456vet-alfort.fr

                This article was submitted to the journal Frontiers in Cellular and Infection Microbiology.

                Article
                10.3389/fcimb.2014.00029
                3942874
                24634890
                79756d74-edd3-4829-b25e-9fb2a0dc1475
                Copyright © 2014 Vayssier-Taussat, Albina, Citti, Cosson, Jacques, Lebrun, Le Loir, Ogliastro, Petit, Roumagnac and Candresse.

                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) or licensor 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
                : 03 December 2013
                : 15 February 2014
                Page count
                Figures: 1, Tables: 0, Equations: 0, References: 70, Pages: 7, Words: 6219
                Categories
                Microbiology
                Review Article

                Infectious disease & Microbiology
                next generation sequencing,microbial ecosystem,interactions

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