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      The Inner Workings of the Outer Surface: Skin and Gill Microbiota as Indicators of Changing Gut Health in Yellowtail Kingfish

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          Abstract

          The mucosal surfaces and associated microbiota of fish are an important primary barrier and provide the first line of defense against potential pathogens. An understanding of the skin and gill microbial assemblages and the factors which drive their composition may provide useful insights into the broad dynamics of fish host–microbial relationships, and may reveal underlying changes in health status. This is particularly pertinent to cultivated systems whereby various stressors may led to conditions (like enteritis) which impinge on productivity. As an economically important species, we assessed whether the outer-surface bacterial communities reflect a change in gut health status of cultivated Yellowtail Kingfish ( Seriola lalandi). Active bacterial assemblages were surveyed from RNA extracts from swabs of the skin and gills by constructing Illumina 16S rRNA gene amplicon libraries. Proteobacteria and Bacteroidetes were predominant in both the skin and gills, with enrichment of key β-proteobacteria in the gills (Nitrosomonadales and Ferrovales). Fish exhibiting early stage chronic lymphocytic enteritis comprised markedly different global bacterial assemblages compared to those deemed healthy and exhibiting late stages of the disease. This corresponded to an overall loss of diversity and enrichment of Proteobacteria and Actinobacteria, particularly in the gills. In contrast, bacterial assemblages of fish with late stage enteritis were generally similar to those of healthy individuals, though with some distinct taxa. In conclusion, gut health status is an important factor which defines the skin and gill bacterial assemblages of fish and likely reflects changes in immune states and barrier systems during the early onset of conditions like enteritis. This study represents the first to investigate the microbiota of the outer mucosal surfaces of fish in response to underlying chronic gut enteritis, revealing potential biomarkers for assessing fish health in commercial aquaculture systems.

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          The SILVA ribosomal RNA gene database project: improved data processing and web-based tools

          SILVA (from Latin silva, forest, http://www.arb-silva.de) is a comprehensive web resource for up to date, quality-controlled databases of aligned ribosomal RNA (rRNA) gene sequences from the Bacteria, Archaea and Eukaryota domains and supplementary online services. The referred database release 111 (July 2012) contains 3 194 778 small subunit and 288 717 large subunit rRNA gene sequences. Since the initial description of the project, substantial new features have been introduced, including advanced quality control procedures, an improved rRNA gene aligner, online tools for probe and primer evaluation and optimized browsing, searching and downloading on the website. Furthermore, the extensively curated SILVA taxonomy and the new non-redundant SILVA datasets provide an ideal reference for high-throughput classification of data from next-generation sequencing approaches.
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            QIIME allows analysis of high-throughput community sequencing data.

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              UPARSE: highly accurate OTU sequences from microbial amplicon reads.

              Amplified marker-gene sequences can be used to understand microbial community structure, but they suffer from a high level of sequencing and amplification artifacts. The UPARSE pipeline reports operational taxonomic unit (OTU) sequences with ≤1% incorrect bases in artificial microbial community tests, compared with >3% incorrect bases commonly reported by other methods. The improved accuracy results in far fewer OTUs, consistently closer to the expected number of species in a community.
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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
                15 January 2018
                2017
                : 8
                : 2664
                Affiliations
                [1] 1Aquatic Sciences Centre, South Australian Research and Development Institute , West Beach, SA, Australia
                [2] 2School of Biological Sciences, Flinders University , Adelaide, SA, Australia
                [3] 3Research Group Microbial Interactions and Processes, Helmholtz Centre for Infection Research , Braunschweig, Germany
                [4] 4South Australian Museum , Adelaide, SA, Australia
                [5] 5Department of Fisheries , South Perth, WA, Australia
                [6] 6Future Fisheries Veterinary Service Pty Ltd. , East Ballina, NSW, Australia
                Author notes

                Edited by: Suhelen Egan, University of New South Wales, Australia

                Reviewed by: Harold J. Schreier, University of Maryland, Baltimore County, United States; Rodrigo Costa, Universidade de Lisboa, Portugal

                *Correspondence: Andrew P. A. Oxley, andrew.oxley@ 123456sa.gov.au

                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.2017.02664
                5775239
                29379473
                190c2744-571c-48e0-a722-d21765fbe051
                Copyright © 2018 Legrand, Catalano, Wos-Oxley, Stephens, Landos, Bansemer, Stone, Qin and Oxley.

                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
                : 09 October 2017
                : 21 December 2017
                Page count
                Figures: 8, Tables: 1, Equations: 0, References: 87, Pages: 17, Words: 0
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                skin,gills,mucosal microbiome,enteritis,aquaculture,seriola lalandi,16s rrna
                Microbiology & Virology
                skin, gills, mucosal microbiome, enteritis, aquaculture, seriola lalandi, 16s rrna

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