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      Integration of Transcriptome, Gross Morphology and Histopathology in the Gill of Sea Farmed Atlantic Salmon ( Salmo salar): Lessons From Multi-Site Sampling


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          The gill of teleost fish is a multifunctional organ involved in many physiological processes such as gas exchange, osmotic and ionic regulation, acid-base balance and excretion of nitrogenous waste. Due to its extensive interface with the environment, the gill plays a key role as a primary mucosal defense tissue against pathogens, as manifested by the presence of the gill-associated lymphoid tissue (GIALT). In recent years, the prevalence of multifactorial gill pathologies has increased significantly, causing substantial losses in Atlantic salmon aquaculture. The transition from healthy to unhealthy gill phenotypes and the progression of multifactorial gill pathologies, such as proliferative gill disease (PGD), proliferative gill inflammation (PGI) and complex gill disorder (CGD), are commonly characterized by epithelial hyperplasia, lamellar fusion and inflammation. Routine monitoring for PGD relies on visual inspection and non-invasive scoring of the gill tissue (gross morphology), coupled with histopathological examination of gill sections. To explore the underlying molecular events that are associated with the progression of PGD, we sampled Atlantic salmon from three different marine production sites in Scotland and examined the gill tissue at three different levels of organization: gross morphology with the use of PGD scores (macroscopic examination), whole transcriptome (gene expression by RNA-seq) and histopathology (microscopic examination). Our results strongly suggested that the changes in PGD scores of the gill tissue were not associated with the changes in gene expression or histopathology. In contrast, integration of the gill RNA-seq data with the gill histopathology enabled us to identify common gene expression patterns associated with multifactorial gill disease, independently from the origin of samples. We demonstrated that the gene expression patterns associated with multifactorial gill disease were dominated by two processes: a range of immune responses driven by pro-inflammatory cytokines and the events associated with tissue damage and repair, driven by caspases and angiogenin.

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          Most cited references92

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          Glutathione peroxidases.

          With increasing evidence that hydroperoxides are not only toxic but rather exert essential physiological functions, also hydroperoxide removing enzymes have to be re-viewed. In mammals, the peroxidases inter alia comprise the 8 glutathione peroxidases (GPx1-GPx8) so far identified. Since GPxs have recently been reviewed under various aspects, we here focus on novel findings considering their diverse physiological roles exceeding an antioxidant activity. GPxs are involved in balancing the H2O2 homeostasis in signalling cascades, e.g. in the insulin signalling pathway by GPx1; GPx2 plays a dual role in carcinogenesis depending on the mode of initiation and cancer stage; GPx3 is membrane associated possibly explaining a peroxidatic function despite low plasma concentrations of GSH; GPx4 has novel roles in the regulation of apoptosis and, together with GPx5, in male fertility. Functions of GPx6 are still unknown, and the proposed involvement of GPx7 and GPx8 in protein folding awaits elucidation. Collectively, selenium-containing GPxs (GPx1-4 and 6) as well as their non-selenium congeners (GPx5, 7 and 8) became key players in important biological contexts far beyond the detoxification of hydroperoxides. This article is part of a Special Issue entitled Cellular functions of glutathione. Copyright © 2012 Elsevier B.V. All rights reserved.
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            The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste.

            The fish gill is a multipurpose organ that, in addition to providing for aquatic gas exchange, plays dominant roles in osmotic and ionic regulation, acid-base regulation, and excretion of nitrogenous wastes. Thus, despite the fact that all fish groups have functional kidneys, the gill epithelium is the site of many processes that are mediated by renal epithelia in terrestrial vertebrates. Indeed, many of the pathways that mediate these processes in mammalian renal epithelial are expressed in the gill, and many of the extrinsic and intrinsic modulators of these processes are also found in fish endocrine tissues and the gill itself. The basic patterns of gill physiology were outlined over a half century ago, but modern immunological and molecular techniques are bringing new insights into this complicated system. Nevertheless, substantial questions about the evolution of these mechanisms and control remain.
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              Assessing the effects of climate change on aquatic invasive species.

              Different components of global environmental change are typically studied and managed independently, although there is a growing recognition that multiple drivers often interact in complex and nonadditive ways. We present a conceptual framework and empirical review of the interactive effects of climate change and invasive species in freshwater ecosystems. Climate change is expected to result in warmer water temperatures, shorter duration of ice cover, altered streamflow patterns, increased salinization, and increased demand for water storage and conveyance structures. These changes will alter the pathways by which non-native species enter aquatic systems by expanding fish-culture facilities and water gardens to new areas and by facilitating the spread of species during floods. Climate change will influence the likelihood of new species becoming established by eliminating cold temperatures or winter hypoxia that currently prevent survival and by increasing the construction of reservoirs that serve as hotspots for invasive species. Climate change will modify the ecological impacts of invasive species by enhancing their competitive and predatory effects on native species and by increasing the virulence of some diseases. As a result of climate change, new prevention and control strategies such as barrier construction or removal efforts may be needed to control invasive species that currently have only moderate effects or that are limited by seasonally unfavorable conditions. Although most researchers focus on how climate change will increase the number and severity of invasions, some invasive coldwater species may be unable to persist under the new climate conditions. Our findings highlight the complex interactions between climate change and invasive species that will influence how aquatic ecosystems and their biota will respond to novel environmental conditions.

                Author and article information

                Front Genet
                Front Genet
                Front. Genet.
                Frontiers in Genetics
                Frontiers Media S.A.
                19 June 2020
                : 11
                [1] 1School of Biological Sciences, Institute of Biological and Environmental Sciences, University of Aberdeen , Aberdeen, United Kingdom
                [2] 2Fish Health and Welfare, Marine Scotland Science , Aberdeen, United Kingdom
                [3] 3Centre for Genome-Enabled Biology and Medicine, University of Aberdeen , Aberdeen, United Kingdom
                [4] 4BioMar AS , Trondheim, Norway
                [5] 5Scottish Sea Farms , Stirling, United Kingdom
                Author notes

                Edited by: Dong Xia, Royal Veterinary College (RVC), United Kingdom

                Reviewed by: Aleksei Krasnov, Nofima, Norway; Mark D. Fast, University of Prince Edward Island, Canada

                *Correspondence: Alex Douglas, a.douglas@ 123456abdn.ac.uk
                Samuel A. M. Martin, sam.martin@ 123456abdn.ac.uk

                This article was submitted to Systems Biology, a section of the journal Frontiers in Genetics

                Copyright © 2020 Król, Noguera, Shaw, Costelloe, Gajardo, Valdenegro, Bickerdike, Douglas and Martin.

                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.

                Page count
                Figures: 9, Tables: 6, Equations: 0, References: 117, Pages: 20, Words: 0
                Original Research

                proliferative gill disease,gene expression,rna-seq,immune response,gill inflammation,aquaculture,climate change


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