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      Microbiome Composition and Function in Aquatic Vertebrates: Small Organisms Making Big Impacts on Aquatic Animal Health

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          Abstract

          Aquatic ecosystems are under increasing stress from global anthropogenic and natural changes, including climate change, eutrophication, ocean acidification, and pollution. In this critical review, we synthesize research on the microbiota of aquatic vertebrates and discuss the impact of emerging stressors on aquatic microbial communities using two case studies, that of toxic cyanobacteria and microplastics. Most studies to date are focused on host-associated microbiomes of individual organisms, however, few studies take an integrative approach to examine aquatic vertebrate microbiomes by considering both host-associated and free-living microbiota within an ecosystem. We highlight what is known about microbiota in aquatic ecosystems, with a focus on the interface between water, fish, and marine mammals. Though microbiomes in water vary with geography, temperature, depth, and other factors, core microbial functions such as primary production, nitrogen cycling, and nutrient metabolism are often conserved across aquatic environments. We outline knowledge on the composition and function of tissue-specific microbiomes in fish and marine mammals and discuss the environmental factors influencing their structure. The microbiota of aquatic mammals and fish are highly unique to species and a delicate balance between respiratory, skin, and gastrointestinal microbiota exists within the host. In aquatic vertebrates, water conditions and ecological niche are driving factors behind microbial composition and function. We also generate a comprehensive catalog of marine mammal and fish microbial genera, revealing commonalities in composition and function among aquatic species, and discuss the potential use of microbiomes as indicators of health and ecological status of aquatic ecosystems. We also discuss the importance of a focus on the functional relevance of microbial communities in relation to organism physiology and their ability to overcome stressors related to global change. Understanding the dynamic relationship between aquatic microbiota and the animals they colonize is critical for monitoring water quality and population health.

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          Most cited references189

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          Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2

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            Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences

            Profiling phylogenetic marker genes, such as the 16S rRNA gene, is a key tool for studies of microbial communities but does not provide direct evidence of a community’s functional capabilities. Here we describe PICRUSt (Phylogenetic Investigation of Communities by Reconstruction of Unobserved States), a computational approach to predict the functional composition of a metagenome using marker gene data and a database of reference genomes. PICRUSt uses an extended ancestral-state reconstruction algorithm to predict which gene families are present and then combines gene families to estimate the composite metagenome. Using 16S information, PICRUSt recaptures key findings from the Human Microbiome Project and accurately predicts the abundance of gene families in host-associated and environmental communities, with quantifiable uncertainty. Our results demonstrate that phylogeny and function are sufficiently linked that this ‘predictive metagenomic’ approach should provide useful insights into the thousands of uncultivated microbial communities for which only marker gene surveys are currently available.
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              A communal catalogue reveals Earth’s multiscale microbial diversity

              Our growing awareness of the microbial world’s importance and diversity contrasts starkly with our limited understanding of its fundamental structure. Despite recent advances in DNA sequencing, a lack of standardized protocols and common analytical frameworks impedes comparisons among studies, hindering the development of global inferences about microbial life on Earth. Here we present a meta-analysis of microbial community samples collected by hundreds of researchers for the Earth Microbiome Project. Coordinated protocols and new analytical methods, particularly the use of exact sequences instead of clustered operational taxonomic units, enable bacterial and archaeal ribosomal RNA gene sequences to be followed across multiple studies and allow us to explore patterns of diversity at an unprecedented scale. The result is both a reference database giving global context to DNA sequence data and a framework for incorporating data from future studies, fostering increasingly complete characterization of Earth’s microbial diversity. Supplementary information The online version of this article (doi:10.1038/nature24621) contains supplementary material, which is available to authorized users.
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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
                11 March 2021
                2021
                : 12
                : 567408
                Affiliations
                [1] 1RECETOX, Faculty of Science, Masaryk University , Brno, Czechia
                [2] 2Department of Large Animal Clinical Sciences, University of Florida , Gainesville, FL, United States
                [3] 3Department of Physiological Sciences, University of Florida , Gainesville, FL, United States
                [4] 4Center for Environmental and Human Toxicology, University of Florida , Gainesville, FL, United States
                [5] 5Department of Environmental and Global Health, University of Florida , Gainesville, FL, United States
                [6] 6Univ Angers, Institut Agro, INRAE, IRHS, SFR QUASAV , Angers, France
                Author notes

                Edited by: Christopher John Grim, United States Food and Drug Administration, United States

                Reviewed by: Sucharit Basu Neogi, International Centre for Diarrhoeal Disease Research (ICDDR), Bangladesh; Lauris Evariste, UMR 5245 Laboratoire Ecologie Fonctionnelle et Environnement (ECOLAB), France

                *Correspondence: Marie Simonin, marie.simonin@ 123456inrae.fr

                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.2021.567408
                7995652
                33776947
                aff33a34-6dff-44a6-a201-66796f0fa5d5
                Copyright © 2021 Sehnal, Brammer-Robbins, Wormington, Blaha, Bisesi, Larkin, Martyniuk, Simonin and Adamovsky.

                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
                : 29 May 2020
                : 05 February 2021
                Page count
                Figures: 2, Tables: 1, Equations: 0, References: 190, Pages: 21, Words: 0
                Categories
                Microbiology
                Review

                Microbiology & Virology
                microbiome,fish,aquatic mammals,stressors,biomonitoring,ecosystem health
                Microbiology & Virology
                microbiome, fish, aquatic mammals, stressors, biomonitoring, ecosystem health

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