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Integrating Genomic and Morphological Approaches in Fish Pathology Research Edinburgh Research Explorer Integrating genomic and morphological approaches in fish pathology research Citation for published version: Ronza, P, Robledo Sanchez, D, Bermudez-Otero, R, Losada , AP, Pardo , BG, Martínez, P & Quiroga, MI 2019, 'Integrating genomic and morphological approaches in fish pathology research: The case of turbot (Scophthalmus maximus) enteromomyxosis ' Frontiers in genetics. DOI: 10.3389/fgene.2019.00026 Digital Object Identifier (DOI): 10.3389/fgene.2019.00026 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: Frontiers in genetics General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 05. Apr. 2019 fgene-10-00026 January 29, 2019 Time: 17:2 # 1 REVIEW published: 31 January 2019 doi: 10.3389/fgene.2019.00026 Integrating Genomic and Morphological Approaches in Fish Pathology Research: The Case of Turbot (Scophthalmus maximus) Enteromyxosis Paolo Ronza1*, Diego Robledo2, Roberto Bermúdez1, Ana Paula Losada1, Belén G. Pardo3, Paulino Martínez3 and María Isabel Quiroga1 1 Departamento de Anatomía, Producción Animal y Ciencias Clínicas Veterinarias, Universidade de Santiago de Compostela, Lugo, Spain, 2 Royal (Dick) School of Veterinary Studies, The Roslin Institute, The University of Edinburgh, Midlothian, United Kingdom, 3 Departamento de Zoología, Genética y Antropología Física, Universidade de Santiago de Compostela, Lugo, Spain Enteromyxosis, caused by Enteromyxum scophthalmi, is one of the most devastating diseases stemming from myxozoan parasites in turbot (Scophthalmus maximus L.), being a limiting factor for its production. The disease develops as a cachectic syndrome, Edited by: Nguyen Hong Nguyen, associated to catarrhal enteritis and leukocytic depletion, with morbidity and mortality University of the Sunshine Coast, rates usually reaching 100%. To date, no effective treatment exists and there are Australia different unknown issues concerning its pathogenesis. The gross and microscopic Reviewed by: lesions associated to enteromyxosis have been thoroughly described, and several Timothy D. Leeds, United States Department morphopathological studies have been carried out to elucidate the mechanisms of this of Agriculture, United States host-parasite interaction. More recently, efforts have been focused on a multidisciplinary Lill-Heidi Johansen, Fisheries and Aquaculture Research approach, combining histopathology and transcriptome analysis, which has provided (Nofima), Norway significant advances in the understanding of the pathogenesis of this parasitosis. RNA- *Correspondence: Seq technology was applied at early and advanced stages of the disease on fishes Paolo Ronza histologically evaluated and classified based on their lesional degree. In the same way, [email protected] the transcriptomic data were analyzed in relation to the morphopathological picture and Specialty section: the course of the disease. In this paper, a comprehensive review of turbot enteromyxosis This article was submitted to is presented, starting from the disease description up to the most novel information Livestock Genomics, a section of the journal extracted by an integrated approach on the infection mechanisms and host response. Frontiers in Genetics Further, we discuss ongoing strategies toward a full understanding of host-pathogen Received: 01 August 2018 interaction and the identification of suitable biomarkers for early diagnosis and disease Accepted: 16 January 2019 Published: 31 January 2019 management strategies. Citation: Keywords: Scophthalmus maximus, Myxozoa, pathogenesis, histopathology, transcriptomics Ronza P, Robledo D, Bermúdez R, Losada AP, Pardo BG, Martínez P and Quiroga MI (2019) Integrating INTRODUCTION Genomic and Morphological Approaches in Fish Pathology Research: The Case of Turbot Turbot (Scophthalmus maximus L.) is a flatfish species naturally distributed throughout the (Scophthalmus maximus) European coast, from the Baltic and the Atlantic Ocean up to the Black Sea, being scarce in the Enteromyxosis. Front. Genet. 10:26. Mediterranean Sea (Prado et al., 2018). Fish are important for human diet, being a good source of doi: 10.3389/fgene.2019.00026 high-quality proteins, vitamins, and other essential nutrients, including n-3 polyunsaturated fatty Frontiers in Genetics | www.frontiersin.org 1 January 2019 | Volume 10 | Article 26 fgene-10-00026 January 29, 2019 Time: 17:2 # 2 Ronza et al. Enteromyxosis: Genomic and Morphological Approaches acids (PUFAs) and trace minerals. Flatfish are a group of general protection. Current efforts are focused on obtaining great commercial value, considered as low-fat fish (2–4% fat) more resistant or tolerant broodstock, and for that the genomic with a firm, white, mild tasting flesh, highly accepted by the architecture of resistance to this parasite is being evaluated in consumers (Cerdá and Manchado, 2013; Dong et al., 2018). the framework of the Fishboost EU project (FP7/2007–2013, ref. The reduction of captures caused by fisheries’ exhaustion has 613611). promoted flatfish aquaculture mainly in Europe and Asia, Similarly, enteromyxosis, caused by the myxozoan parasite with turbot and Japanese flounder Paralichthys olivaceus as the Enteromyxum scophthalmi, represents a major challenge to dominant species (Food and Agriculture Organization [FAO], turbot production, with morbidity and mortality rates usually 2016). It is a fast-growing industry, where the high appreciation approaching 100% (Branson et al., 1999; Redondo et al., 2004; by the market allows higher prices, which compensate the Quiroga et al., 2006). Despite efforts to find an effective greater production costs of flatfish due to their land-based treatment against this disease, mainly testing coccidiostatic aquaculture systems (Cerdá and Manchado, 2013; Robledo drugs alone or in combination with antibiotics (Bermúdez et al., 2017a). Turbot, in particular, is a great value species et al., 2006a; Palenzuela et al., 2009a), there are still no that is much favored in many market segments such as available therapeutic measures. Current control measures are white tablecloth restaurants (Bjørndal and Øiestad, 2010). The basically preventive, focused on improving husbandry strategies. aquaculture production of this species started in the late A good treatment (ozone, UV and filtration) is essential for 1970s and has experienced an important increase in the last incoming and effluent water, and periodic epidemiological decade. In the European Union (EU) more than 10,000 tons surveys have been suggested for early detection of the of turbot were produced in 2016, mostly in Spain (>70% infection. Once the presence of E. scophthalmi is detected of EU production), and in particular in Galicia (NW Spain, at farm facilities, the only available option is culling of the 99% of Spanish production; Apromar Asociación Empresarial units where the infection was detected followed by their de Acuicultura de España, 2017). Worldwide aquaculture disinfection to minimize losses (Quiroga et al., 2006; Sitjà- production of turbot rose above 65,000 tons in 2015, mostly Bobadilla and Palenzuela, 2012). Enteromyxosis affects turbot due to its quick expansion in PR China (Martínez et al., weighing over 50 g, with the highest prevalence observed 2016) where the species was introduced in the 1990s (Lei and in the range between 201 and 300 g. Mortality can be Liu, 2010). As for most aquaculture species, and despite being low at the beginning of the outbreak if older fish are first mainly produced in land-based facilities, pathogens represent infected, but increases exponentially and younger fish are the most important threat to the sustainability of turbot progressively affected. A 100% mortality is often observed aquaculture. Although there has been significant progress with in a few weeks, particularly at summer temperatures (water the development of some effective treatments and vaccines or temperature >14◦C), which have been related to a faster the identification of major genomic regions associated with progress of the disease (Quiroga et al., 2006; Sitjà-Bobadilla pathogen resistance (Martínez et al., 2016), diseases represent and Palenzuela, 2012). On the other hand, turbot enteromyxosis the main challenge that turbot farming will face in the near is generally characterized by a long pre-patent period. The future. first clinical signs appear and the parasite is detected several Bacterial diseases, such as tenacibaculosis by Tenacibaculum weeks after the exposure (Redondo et al., 2004; Quiroga maritimum, vibriosis by Vibrio anguillarum, edwarsiellosis et al., 2006). Some evidences of resistance to this parasite by Edwardsiella tarda, and aeromoniasis (furunculosis) by have been reported; the origin of turbot was identified as a Aeromonas salmonicida subsp. salmonicida, are among the most risk factor (Quiroga et al., 2006), and cases of fish showing common
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