Partial or total replacement of fish meal by a mixture of plant protein (PP) sources (corn gluten, wheat gluten, extruded peas, rapeseed meal and sweet white lupin) balanced with indispensable amino acids was examined in juvenile gilthead sea bream over the course of a 6-month growth trial. A diet with fish meal (FM) as the sole protein source was compared to diets with 50%, 75% and 100% of replacement (PP50, PP75, and PP100). The possible influence of diets on growth performance, plasma metabolites, gut integrity, liver structure, anti-oxidant and immune status was evaluated. Final body weight was progressively decreased with PP inclusion, but in PP50 and PP75-fed fish, feed efficiency (FE) was significantly improved and specific growth rates remained unchanged or slightly reduced in comparison to fish fed the FM diet. In fish fed PP100 diet, FE remained unchanged and feed intake and growth decreased dramatically. In this group of fish, liver fat deposition was also largely increased, enterocytes showed an increased number of lipidic vacuoles and/or deposition of protein droplets, and the submucosa of intestine was dilated/hypertrophied and infiltrated with eosinophilic granular cells. Plasma glucose levels did not differ among the four groups, but a significant and progressive decrease of plasma cholesterol and plasma protein levels was found with FM replacement. The glutathione redox status in blood and liver increased with the increase of PP content and this increment was statistically significant in the liver of the three PP-fed groups. Glutathione reductase and γ-glutamyl transferase were also enhanced by PP inclusion. Plasma lysozyme levels were not altered by the dietary treatment, but respiratory burst of head kidney leucocytes and plasma myeloperoxidase values were significantly increased in PP75 and PP100 fish, respectively. Complement (ACH50) was significantly increased in PP50 fed fish and decreased in PP75 and PP100 groups. As a general conclusion, substitution of FM by a mixture of PP sources exerted an anti-oxidative effect, compromised growth performance only at the 100% level, and decreased one of the immune defence mechanisms at above 75% level.

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BackgroundThe constant increase of aquaculture production and wealthy seafood consumption has forced the industry to explore alternative and more sustainable raw aquafeed materials, and plant ingredients have been used to replace marine feedstuffs in many farmed fish. The objective of the present study was to assess whether plant-based diets can induce changes in the intestinal mucus proteome, gut autochthonous microbiota and disease susceptibility of fish, and whether these changes could be reversed by the addition of sodium butyrate to the diets. Three different trials were performed using the teleostean gilthead sea bream (Sparus aurata) as model. In a first preliminary short-term trial, fish were fed with the additive (0.8%) supplementing a basal diet with low vegetable inclusion (D1) and then challenged with a bacteria to detect possible effects on survival. In a second trial, fish were fed with diets with greater vegetable inclusion levels (D2, D3) and the long-term effect of sodium butyrate at a lower dose (0.4%) added to D3 (D4 diet) was tested on the intestinal proteome and microbiome. In a third trial, the long-term effectiveness of sodium butyrate (D4) to prevent disease outcome after an intestinal parasite (Enteromyxum leei) challenge was tested.ResultsThe results showed that opposed forces were driven by dietary plant ingredients and sodium butyrate supplementation in fish diet. On the one hand, vegetable diets induced high parasite infection levels that provoked drops in growth performance, decreased intestinal microbiota diversity, induced the dominance of the Photobacterium genus, as well as altered the gut mucosal proteome suggesting detrimental effects on intestinal function. On the other hand, butyrate addition slightly decreased cumulative mortality after bacterial challenge, avoided growth retardation in parasitized fish, increased intestinal microbiota diversity with a higher representation of butyrate-producing bacteria and reversed most vegetable diet-induced changes in the gut proteome.ConclusionsThis integrative work gives insights on the pleiotropic effects of a dietary additive on the restoration of intestinal homeostasis and disease resilience, using a multifaceted approach.Electronic supplementary materialThe online version of this article (10.1186/s40168-017-0390-3) contains supplementary material, which is available to authorized users.

The feasibility of fish oil (FO) replacement by vegetable oils (VO) was investigated in gilthead sea bream (Sparus aurata L.) in a growth trial conducted for the duration of 8 months. Four isolipidic and isoproteic diets rich in plant proteins were supplemented with L-lysine (0·55 %) and soya lecithin (1 %). Added oil was either FO (control) or a blend of VO, replacing 33 % (33VO diet), 66 % (66VO diet) and 100 % (VO diet) of FO. No detrimental effects on growth performance were found with the partial FO replacement, but feed intake and growth rates were reduced by about 10 % in fish fed the VO diet. The replacement strategy did not damage the intestinal epithelium, and massive accumulation of lipid droplets was not found within enterocytes. All fish showed fatty livers, but signs of lipoid liver disease were only found in fish fed the VO diet. Muscle fatty acid profiles of total lipids reflected the diet composition with a selective incorporation of unsaturated fatty acids in polar lipids. The robustness of the phospholipid fatty acid profile when essential fatty acid requirements were theoretically covered by the diet was evidenced by multivariate principal components analysis in fish fed control, 33VO and 66VO diets.

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Growth performance and growth regulatory pathways were examined in juvenile gilthead sea bream fed diets containing largely plant-based ingredients. Four isonitrogenous and isolipidic extruded diets with a low level (20%) of fish meal inclusion were formulated with graded levels of a vegetable oil mixture (17:58:25 of rapeseed: linseed: palm oils) replacing fish oil at 33, 66 and 100% (33VO, 66VO and VO diets). All diets were supplemented with lysine (0.55%) and contained soy lecithin (1%). Daily growth coefficients and feed efficiency over the course of an 11-week trial were almost identical in fish fed the FO, 33VO and 66VO diets. The VO diet reduced feed intake and growth without significant effects in proximate whole body composition, nitrogen or energy retentions. The highest concentration of plasma levels of insulin-like growth factor-I (IGF-I) was found in fish fed the 33VO diet. The lowest concentration was attained in fish fed the VO diet, whereas intermediate values were found in fish fed FO and 66VO diets. An opposite trend was found for circulating levels of growth hormone (GH), probably as a result of a reduced negative feedback inhibition from circulating IGF-I. Hepatic expression of IGF-I and GH receptor type I (GHR-I) was regulated in concert and mRNA levels paralleled plasma levels of IGF-I. Hepatic IGF-II and GHR-II were expressed in a more constitutive manner and no changes at the mRNA level were detected. In the skeletal muscle, IGF-I and GHR-I mRNAs did not vary significantly among groups. By contrast, IGF-II mRNA was up-regulated in fish fed the control diet, whereas the highest amount of GHR-II mRNA was attained in fish fed the 66VO diet. All together, these results suggest different growth compensatory mechanisms mediated by IGF-II and GHR-II at the local tissue level. These new insights prompted us to propose that practical diets low in marine ingredients can be used over the productive cycle of gilthead sea bream when essential fatty acids are supplied above the requirement levels.

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