Abstract
BackgroundThe achievement of sustainable feeding practices in aquaculture by reducing the reliance on wild-captured fish, via replacement of fish-based feed with plant-based feed, is impeded by the poor growth response seen in fish fed high levels of plant ingredients. Our recent strategy to nutritionally program rainbow trout by early short-term exposure to a plant-based (V) diet versus a control fish-based (M) diet at the first-feeding fry stage when the trout fry start to consume exogenous feed, resulted in remarkable improvements in feed intake, growth and feed utilization when the same fish were challenged with the diet V (V-challenge) at the juvenile stage, several months following initial exposure. We employed microarray expression analysis at the first-feeding and juvenile stages to deduce the mechanisms associated with the nutritional programming of plant-based feed acceptance in trout.ResultsTranscriptomic analysis was performed on rainbow trout whole fry after 3 weeks exposure to either diet V or diet M at the first feeding stage (3-week), and in the whole brain and liver of juvenile trout after a 25 day V-challenge, using a rainbow trout custom oligonucleotide microarray. Overall, 1787 (3-week + Brain) and 924 (3-week + Liver) mRNA probes were affected by the early-feeding exposure. Gene ontology and pathway analysis of the corresponding genes revealed that nutritional programming affects pathways of sensory perception, synaptic transmission, cognitive processes and neuroendocrine peptides in the brain; whereas in the liver, pathways mediating intermediary metabolism, xenobiotic metabolism, proteolysis, and cytoskeletal regulation of cell cycle are affected. These results suggest that the nutritionally programmed enhanced acceptance of a plant-based feed in rainbow trout is driven by probable acquisition of flavour and feed preferences, and reduced sensitivity to changes in hepatic metabolic and stress pathways.ConclusionsThis study outlines the molecular mechanisms in trout brain and liver that accompany the nutritional programming of plant-based diet acceptance in trout, reinforces the notion of the first-feeding stage in oviparous fish as a critical window for nutritional programming, and provides support for utilizing this strategy to achieve improvements in sustainability of feeding practices in aquaculture.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2804-1) contains supplementary material, which is available to authorized users.
Highlights
The achievement of sustainable feeding practices in aquaculture by reducing the reliance on wild-captured fish, via replacement of fish-based feed with plant-based feed, is impeded by the poor growth response seen in fish fed high levels of plant ingredients
Expression profiling The present study aims to identify the molecular mechanisms that govern the positive effect of prior plant-diet exposure on the acceptance of the same plant-diet when given 7 months later
Our results elaborate the transcriptomic changes in trout fry at the first-feeding stage, and in the brain and liver of juvenile trout, accompanying the nutritional programming that enhances feed acceptance of a plantbased diet in rainbow trout
Summary
The achievement of sustainable feeding practices in aquaculture by reducing the reliance on wild-captured fish, via replacement of fish-based feed with plant-based feed, is impeded by the poor growth response seen in fish fed high levels of plant ingredients. Achieving independence on wild fish-derived feed inputs is a priority for the aquaculture industry to ensure its further sustainable growth [1] In this respect, the reduced growth performance seen in farmed fish, including rainbow trout, when fed high levels of plant-based ingredients in lieu of fishery-derived fish meal and fish oil is a problem [2, 3]. In order to analyse the metabolic consequences of partial or complete substitution of fishmeal and fish oil with plant-based sources, studies based on nutrigenomic approaches have been undertaken, comparing hepatic transcriptome changes in trout fed fishmeal or fish oilfree diets [5], total replacement of fishmeal or fish oil with plant sources in trout [6] and European sea bass [7], fishmeal substitution with plant proteins in Atlantic salmon [8], and a proteomic study on the effect of plantprotein substitution on hepatic metabolism in trout [9] Taken together, these studies showed that plant-feeding altered the expression of actors involved in a large variety of biological functions. Strategies to overcome the poor acceptance of plant-based ingredients in trout have included the use of selective breeding techniques to select for fish with a greater ability to grow on plant-based feeds [15,16,17]
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