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Long-term feeding a plant-based diet devoid of marine ingredients strongly affects certain key metabolic enzymes in the rainbow trout liver

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Abstract

Incorporation of a plant blend in the diet can affect growth parameters and metabolism in carnivorous fish. We studied for the first time the long-term (1 year) metabolic response of rainbow trout fed from first feeding with a plant-based diet totally devoid of marine ingredients. Hepatic enzymes were analyzed at enzymatic and molecular levels, at 3, 8 and 24 h after the last meal to study both the short-term effects of the last meal and long-term effects of the diet. The results were compared with those of fish fed a control diet of fish meal and fish oil. Growth, feed intake, feed efficiency and protein retention were lower in the group fed the plant-based diet. Glucokinase and pyruvate kinase activity were lower in the livers of trout fed the plant-based diet which the proportion of starch was lower than in the control diet. Glutamate dehydrogenase was induced by the plant-based diet, suggesting an imbalance of amino acids and a possible link with the lower protein retention observed. Gene expression of delta 6 desaturase was higher in fish fed the plant-based diet, probably linked to a high dietary level of linolenic acid and the absence of long-chain polyunsaturated fatty acids in vegetable oils. Hydroxymethylglutaryl-CoA synthase expression was also induced by plant-based diet because of the low rate of cholesterol in the diet. Changes in regulation mechanisms already identified through short-term nutritional experiments (<12 weeks) suggest that metabolic responses are implemented at short term and remain in the long term.

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Abbreviations

M diet:

Marine resources-based diet

PB diet:

Plant-based diet

GK:

Glucokinase

PK:

Pyruvate kinase

G6Pase:

Glucose 6 phosphatase

GDH:

Glutamate dehydrogenase

ASAT:

Aspartate aminotransferase

ALAT:

Alanine aminotransferase

CS:

Citrate synthase

FAS:

Fatty acid synthase

HOAD:

3-Hydroxyacyl-CoA dehydrogenase

D6D:

Delta6desaturase

HMGCS:

Hydroxymethylglutaryl-CoA synthase

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Acknowledgments

We thank Thierry Kerneis who managed the trial at the PEIMA experimental fish farm, Frederic Terrier and Frank Sandres for the preparation of the two experimental diets in Donzacq INRA experimental facilities, and Alexandre Herman for plasma analysis.

Funding

This research was funded by the FUI (Fond Unique Interministériel) Vege-Aqua (2009–2012) and by the European Commission (European project FP7-KBBE-2001 N°288925 ARRAINA for Advanced Research Initiatives for Nutrition and Aquaculture).

Author contributions

The contributions of the authors to the study were as follow: R.L.B., M.D.N., E.Q. and F.M. conceived and designed the experiments. L.L. supervised the in vivo trial. F.M., R.L.B. and L.L. designed and performed samplings. V.V. and R.L.B. performed all the analysis. V.V. and RLB. analyzed the data. V.V., S.P. and F.M. wrote the paper. All authors read and approved the final manuscript.

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Authors and Affiliations

  1. INRA UR 1067 NuMeA (Nutrition Metabolism Aquaculture), Aquapôle, 64310, Saint Pée Sur Nivelle, France

    Vincent Véron, Stéphane Panserat & Françoise Médale

  2. INRA, UMR1313 GABI (Génétique animale et biologie intégrative), Jouy-En-Josas, France

    Richard Le Boucher, Edwige Quillet & Mathilde Dupont-Nivet

  3. INRA, UE 0937 PEIMA (Pisciculture Expérimentale INRA des Monts d’Arrée), Sizun, France

    Laurent Labbé

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  1. Vincent Véron
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  2. Stéphane Panserat
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  3. Richard Le Boucher
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  4. Laurent Labbé
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  5. Edwige Quillet
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  6. Mathilde Dupont-Nivet
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  7. Françoise Médale
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Correspondence to Vincent Véron.

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Véron, V., Panserat, S., Le Boucher, R. et al. Long-term feeding a plant-based diet devoid of marine ingredients strongly affects certain key metabolic enzymes in the rainbow trout liver. Fish Physiol Biochem 42, 771–785 (2016). https://doi.org/10.1007/s10695-015-0174-2

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