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      Dietary vegetable oils do not alter the intestine transcriptome of gilthead sea bream ( Sparus aurata), but modulate the transcriptomic response to infection with Enteromyxum leei

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          Abstract

          Background

          Studies conducted with gilthead sea bream ( Sparus aurata L.) have determined the maximum dietary replacement of fish meal and oil without compromising growth or product quality. The present study aimed to analyze the effect of the nutritional background on fish health and fish fed plant protein-based diets with fish oil (FO diet) or a blend of vegetable oils (66VO diet) were exposed for 102 days to the intestinal myxosporean parasite Enteromyxum leei, and the intestine transcriptome was analyzed with a customized oligo-microarray of 7,500 annotated genes.

          Results

          Infection prevalence was high and similar in the two diet groups, but the outcome of the disease was more pronounced in fish fed the 66VO diet. No differences were found in the transcriptome of both diet control groups, whereas the number of differentially expressed genes in infected groups was considerable. K-means clustering of these differentially expressed genes identified four expression patterns that reflected the progression of the disease with the magnitude of the fold-change being higher in infected 66VO fish. A positive correlation was found between the time of infection and the magnitude of the transcriptional change within the 66VO group, being higher in early infected animals. Within this diet group, a strong up-regulation of many components of the immune specific response was evidenced, whereas other genes related to complement response and xenobiotic metabolism were down-regulated.

          Conclusions

          The high replacement of fish oil by vegetable oils in practical fish feeds did not modify the intestine transcriptome of gilthead sea bream, but important changes were apparent when fish were exposed to the myxosporean E. leei. The detected changes were mostly a consequence rather than a cause of the different disease progression in the two diet groups. Hence, the developed microarray constitutes an excellent diagnostic tool to address changes associated with the action of intestinal pathogens, but lacks a prognostic value to predict in advance the different susceptibility of growing fish to the current pathogen.

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          Most cited references59

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          Innate immunity of fish (overview).

          The innate immune system is the only defence weapon of invertebrates and a fundamental defence mechanism of fish. The innate system also plays an instructive role in the acquired immune response and homeostasis and is therefore equally important in higher vertebrates. The innate system's recognition of non-self and danger signals is served by a limited number of germ-line encoded pattern recognition receptors/proteins, which recognise pathogen associated molecular patterns like bacterial and fungal glycoproteins and lipopolysaccharides and intracellular components released through injury or infection. The innate immune system is divided into physical barriers, cellular and humoral components. Humoral parameters include growth inhibitors, various lytic enzymes and components of the complement pathways, agglutinins and precipitins (opsonins, primarily lectins), natural antibodies, cytokines, chemokines and antibacterial peptides. Several external and internal factors can influence the activity of innate immune parameters. Temperature changes, handling and crowding stress can have suppressive effects on innate parameters, whereas several food additives and immunostimulants can enhance different innate factors. There is limited data available about the ontogenic development of the innate immunological system in fish. Active phagocytes, complement components and enzyme activity, like lysozyme and cathepsins, are present early in the development, before or soon after hatching.
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            Teleost intestinal immunology.

            Teleosts clearly have a more diffuse gut associated lymphoid system, which is morphological and functional clearly different from the mammalian GALT. All immune cells necessary for a local immune response are abundantly present in the gut mucosa of the species studied and local immune responses can be monitored after intestinal immunization. Fish do not produce IgA, but a special mucosal IgM isotype seems to be secreted and may (partly) be the recently described IgZ/IgT. Fish produce a pIgR in their mucosal tissues but it is smaller (2 ILD) than the 4-5 ILD pIgR of higher vertebrates. Whether teleost pIgR is transcytosed and cleaved off in the same way needs further investigation, especially because a secretory component (SC) is only reported in one species. Teleosts also have high numbers of IEL, most of them are CD3-ɛ+/CD8-α+ and have cytotoxic and/or regulatory function. Possibly many of these cells are TCRγδ cells and they may be involved in the oral tolerance induction observed in fish. Innate immune cells can be observed in the teleost gut from first feeding onwards, but B cells appear much later in mucosal compartments compared to systemic sites. Conspicuous is the very early presence of putative T cells or their precursors in the fish gut, which together with the rag-1 expression of intestinal lymphoid cells may be an indication for an extra-thymic development of certain T cells. Teleosts can develop enteritis in their antigen transporting second gut segment and epithelial cells, IEL and eosinophils/basophils seem to play a crucial role in this intestinal inflammation model. Teleost intestine can be exploited for oral vaccination strategies and probiotic immune stimulation. A variety of encapsulation methods, to protect vaccines against degradation in the foregut, are reported with promising results but in most cases they appear not to be cost effective yet. Microbiota in fish are clearly different from terrestrial animals. In the past decade a fast increasing number of papers is dedicated to the oral administration of a variety of probiotics that can have a strong health beneficial effect, but much more attention has to be paid to the immune mechanisms behind these effects. The recent development of gnotobiotic fish models may be very helpful to study the immune effects of microbiota and probiotics in teleosts. Copyright © 2010 Elsevier Ltd. All rights reserved.
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              Nutrition and health of aquaculture fish.

              Under intensive culture conditions, fish are subject to increased stress owing to environmental (water quality and hypoxia) and health conditions (parasites and infectious diseases). All these factors have negative impacts on fish well-being and overall performance, with consequent economic losses. Though good management practices contribute to reduce stressor effects, stress susceptibility is always high under crowded conditions. Adequate nutrition is essential to avoid deficiency signs, maintain adequate animal performance and sustain normal health. Further, it is becoming evident that diets overfortified with specific nutrients [amino acids, essential fatty acids (FAs), vitamins or minerals] at levels above requirement may improve health condition and disease resistance. Diet supplements are also being evaluated for their antioxidant potential, as fish are potentially at risk of peroxidative attack because of the large quantities of highly unsaturated FAs in both fish tissues and diets. Functional constituents other than essential nutrients (such as probiotics, prebiotics and immunostimulants) are also currently being considered in fish nutrition aiming to improve fish growth and/or feed efficiency, health status, stress tolerance and resistance to diseases. Such products are becoming more and more important for reducing antibiotic utilization in aquafarms, as these have environmental impacts, may accumulate in animal tissues and increase bacterial resistance. This study reviews knowledge of the effect of diet nutrients on health, welfare and improvement of disease resistance in fish. © 2012 Blackwell Publishing Ltd.
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                Author and article information

                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central
                1471-2164
                2012
                11 September 2012
                : 13
                : 470
                Affiliations
                [1 ]Nutrigenomics and Fish Growth Endocrinology Group, Department of Marine Species Biology, Culture and Pathology, Instituto de Acuicultura Torre de la Sal (IATS-CSIC), Ribera de Cabanes, Castellón, 12595, Spain
                [2 ]Fish Pathology Group, Department of Marine Species Biology, Culture and Pathology, Instituto de Acuicultura Torre de la Sal (IATS-CSIC), Ribera de Cabanes, Castellón, 12595, Spain
                [3 ]Ryan Institute, National University of Ireland, Galway, Ireland
                [4 ]INRA, UR1067 NuMeA Nutrition, Metabolism Aquaculture, Saint Pée-sur, Nivelle, F64310, France
                Article
                1471-2164-13-470
                10.1186/1471-2164-13-470
                3444936
                22967181
                23d28215-657f-4420-94a1-822452b93760
                Copyright ©2012 Calduch-Giner et al.; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 1 June 2012
                : 7 September 2012
                Categories
                Research Article

                Genetics
                nutrigenomics,transcriptome,parasite,intestine,teleost,myxozoa
                Genetics
                nutrigenomics, transcriptome, parasite, intestine, teleost, myxozoa

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