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      Defining the Distinct Skin and Gut Microbiomes of the Northern Pike ( Esox lucius)

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          Abstract

          The microbiome of freshwater fish has important implications for both commercial and recreational fishing because it can have significant impacts on host heath, spoilage rates, and susceptibility to disease. The aqueous environment serves as a possible avenue for continuous introduction of microbes to an animal host, but little is known about how the surrounding microbiota contribute to piscine microbiomes. To better understand the composition of the fish microbiome exposed to the natural environment, we profiled the microbial composition of the gut and the skin mucosal surface (SMS) of northern pike ( Esox lucius) and the surrounding river water. We collected fish samples from eight sites along a single river in southwestern Quebec, Canada and analyzed the microbial composition via 16S rRNA sequencing. Our results reveal robust taxonomic differences between the SMS and the gut, indicating a divergence between the microbiomes. The gut community was characterized by a lower alpha diversity compared to the SMS and a large proportion of Cetobacterium, a genus previously linked to carnivorous species. On the other hand, the SMS was more similar to the water than the gut at the family level but divergent at lower taxonomic levels, with fewer than 30% of amplicon sequence variants (ASVs) shared between the SMS and water. In total, our results suggest the establishment of distinct communities across the two fish sites, as well as a clear separation from the microbes in surrounding waters. These data indicate that despite continuous exposure to water, pike are able to establish and maintain unique microbial communities.

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          Most cited references64

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          Environmental and ecological factors that shape the gut bacterial communities of fish: a meta-analysis.

          Symbiotic bacteria often help their hosts acquire nutrients from their diet, showing trends of co-evolution and independent acquisition by hosts from the same trophic levels. While these trends hint at important roles for biotic factors, the effects of the abiotic environment on symbiotic community composition remain comparably understudied. In this investigation, we examined the influence of abiotic and biotic factors on the gut bacterial communities of fish from different taxa, trophic levels and habitats. Phylogenetic and statistical analyses of 25 16S rRNA libraries revealed that salinity, trophic level and possibly host phylogeny shape the composition of fish gut bacteria. When analysed alongside bacterial communities from other environments, fish gut communities typically clustered with gut communities from mammals and insects. Similar consideration of individual phylotypes (vs. communities) revealed evolutionary ties between fish gut microbes and symbionts of animals, as many of the bacteria from the guts of herbivorous fish were closely related to those from mammals. Our results indicate that fish harbour more specialized gut communities than previously recognized. They also highlight a trend of convergent acquisition of similar bacterial communities by fish and mammals, raising the possibility that fish were the first to evolve symbioses resembling those found among extant gut fermenting mammals. © 2012 Blackwell Publishing Ltd.
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            Teleost microbiomes: the state of the art in their characterization, manipulation and importance in aquaculture and fisheries

            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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              Progress in fish gastrointestinal microbiota research

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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
                12 September 2019
                2019
                : 10
                : 2118
                Affiliations
                Department of Molecular Microbiology and Immunology, Division of Biology and Medicine, Brown University , Providence, RI, United States
                Author notes

                Edited by: David William Waite, The University of Auckland, New Zealand

                Reviewed by: Zoe Adina Pratte, Georgia Institute of Technology, United States; Raquel Xavier, University of Porto, Portugal

                *Correspondence: Peter Belenky, peter_belenky@ 123456brown.edu

                These authors have contributed equally to this work

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

                Article
                10.3389/fmicb.2019.02118
                6751255
                31572326
                3cdd5b77-92ca-4e86-87eb-0f4b032bdb95
                Copyright © 2019 Reinhart, Korry, Rowan-Nash and Belenky.

                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
                : 23 May 2019
                : 28 August 2019
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 91, Pages: 11, Words: 0
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                fish,microbiota,cetobacterium,16s rrna,aquatic,carnivore,communities,next-generation sequencing

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