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      Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries

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          Abstract

          Indigenous microbiota play a critical role in the lives of their vertebrate hosts. In human and mouse models it is increasingly clear that innate and adaptive immunity develop in close concert with the commensal microbiome. Furthermore, several aspects of digestion and nutrient metabolism are governed by intestinal microbiota. Research on teleosts has responded relatively slowly to the introduction of massively parallel sequencing procedures in microbiomics. Nonetheless, progress has been made in biotic and gnotobiotic zebrafish models, defining a core microbiome and describing its role in development. However, microbiome research in other teleost species, especially those important from an aquaculture perspective, has been relatively slow. In this review, we examine progress in teleost microbiome research to date. We discuss teleost microbiomes in health and disease, microbiome ontogeny, prospects for successful microbiome manipulation (especially in an aquaculture setting) and attempt to identify important future research themes. We predict an explosion in research in this sector in line with the increasing global demand for fish protein, and the need to find sustainable approaches to improve aquaculture yield. The reduced cost and increasing ease of next generation sequencing technologies provides the technological backing, and the next 10 years will be an exciting time for teleost microbiome research.

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          Most cited references 105

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          Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis.

          Toll-like receptors (TLRs) play a crucial role in host defense against microbial infection. The microbial ligands recognized by TLRs are not unique to pathogens, however, and are produced by both pathogenic and commensal microorganisms. It is thought that an inflammatory response to commensal bacteria is avoided due to sequestration of microflora by surface epithelia. Here, we show that commensal bacteria are recognized by TLRs under normal steady-state conditions, and this interaction plays a crucial role in the maintenance of intestinal epithelial homeostasis. Furthermore, we find that activation of TLRs by commensal microflora is critical for the protection against gut injury and associated mortality. These findings reveal a novel function of TLRs-control of intestinal epithelial homeostasis and protection from injury-and provide a new perspective on the evolution of host-microbial interactions.
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            Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors.

            In vertebrates, including humans, individuals harbor gut microbial communities whose species composition and relative proportions of dominant microbial groups are tremendously varied. Although external and stochastic factors clearly contribute to the individuality of the microbiota, the fundamental principles dictating how environmental factors and host genetic factors combine to shape this complex ecosystem are largely unknown and require systematic study. Here we examined factors that affect microbiota composition in a large (n = 645) mouse advanced intercross line originating from a cross between C57BL/6J and an ICR-derived outbred line (HR). Quantitative pyrosequencing of the microbiota defined a core measurable microbiota (CMM) of 64 conserved taxonomic groups that varied quantitatively across most animals in the population. Although some of this variation can be explained by litter and cohort effects, individual host genotype had a measurable contribution. Testing of the CMM abundances for cosegregation with 530 fully informative SNP markers identified 18 host quantitative trait loci (QTL) that show significant or suggestive genome-wide linkage with relative abundances of specific microbial taxa. These QTL affect microbiota composition in three ways; some loci control individual microbial species, some control groups of related taxa, and some have putative pleiotropic effects on groups of distantly related organisms. These data provide clear evidence for the importance of host genetic control in shaping individual microbiome diversity in mammals, a key step toward understanding the factors that govern the assemblages of gut microbiota associated with complex diseases.
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              Evidence for a core gut microbiota in the zebrafish.

              Experimental analysis of gut microbial communities and their interactions with vertebrate hosts is conducted predominantly in domesticated animals that have been maintained in laboratory facilities for many generations. These animal models are useful for studying coevolved relationships between host and microbiota only if the microbial communities that occur in animals in lab facilities are representative of those that occur in nature. We performed 16S rRNA gene sequence-based comparisons of gut bacterial communities in zebrafish collected recently from their natural habitat and those reared for generations in lab facilities in different geographic locations. Patterns of gut microbiota structure in domesticated zebrafish varied across different lab facilities in correlation with historical connections between those facilities. However, gut microbiota membership in domesticated and recently caught zebrafish was strikingly similar, with a shared core gut microbiota. The zebrafish intestinal habitat therefore selects for specific bacterial taxa despite radical differences in host provenance and domestication status.
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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
                02 June 2014
                2014
                : 5
                Affiliations
                1Département de Biologie, Institut de Biologie Intégrative et des Systèmes, Université Laval Québec, QC, Canada
                2Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, University of Wales Bangor, UK
                3Department of Fisheries, Gorgan University of Agricultural Sciences and Natural Resources Gorgan, Iran
                Author notes

                Edited by: David Georges Biron, Centre National de la Recherche Scientifique, France

                Reviewed by: Ryan J. Newton, University of Wisconsin-Milwaukee, USA; Jaime Romero, Universidad de Chile, Chile

                *Correspondence: Nicolas Derome, Département de Biologie, Institut de Biologie Intégrative et des Systèmes, Université Laval, Pavillon Alexandre-Vachon, 1045, av. de la Medecine, Local 3058, Québec, QC G1V 0A6, Canada e-mail: nicolas.derome@ 123456bio.ulaval.ca

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

                †These authors have contributed equally to this work.

                Article
                10.3389/fmicb.2014.00207
                4040438
                Copyright © 2014 Llewellyn, Boutin, Hoseinifar and Derome.

                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.

                Page count
                Figures: 3, Tables: 1, Equations: 0, References: 149, Pages: 17, Words: 11632
                Categories
                Microbiology
                Review Article

                Microbiology & Virology

                fisheries, aquaculture, probiotics, microbiota, fish

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