Under control: how a dietary additive can restore the gut microbiome and proteomic profile, and improve disease resilience in a marine teleostean fish fed vegetable diets

Abstract Background The 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...

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Main Authors: María Carla Piazzon, Josep Alvar Calduch-Giner, Belén Fouz, Itziar Estensoro, Paula Simó-Mirabet, Mónica Puyalto, Vasileios Karalazos, Oswaldo Palenzuela, Ariadna Sitjà-Bobadilla, Jaume Pérez-Sánchez
Format: Article
Language:English
Published: BMC 2017-12-01
Series:Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40168-017-0390-3
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author María Carla Piazzon
Josep Alvar Calduch-Giner
Belén Fouz
Itziar Estensoro
Paula Simó-Mirabet
Mónica Puyalto
Vasileios Karalazos
Oswaldo Palenzuela
Ariadna Sitjà-Bobadilla
Jaume Pérez-Sánchez
author_facet María Carla Piazzon
Josep Alvar Calduch-Giner
Belén Fouz
Itziar Estensoro
Paula Simó-Mirabet
Mónica Puyalto
Vasileios Karalazos
Oswaldo Palenzuela
Ariadna Sitjà-Bobadilla
Jaume Pérez-Sánchez
author_sort María Carla Piazzon
collection DOAJ
description Abstract Background The 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. Results The 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. Conclusions This 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.
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spelling doaj.art-97b598ee84424e9da73f1bf6220bec032022-12-21T18:53:55ZengBMCMicrobiome2049-26182017-12-015112310.1186/s40168-017-0390-3Under control: how a dietary additive can restore the gut microbiome and proteomic profile, and improve disease resilience in a marine teleostean fish fed vegetable dietsMaría Carla Piazzon0Josep Alvar Calduch-Giner1Belén Fouz2Itziar Estensoro3Paula Simó-Mirabet4Mónica Puyalto5Vasileios Karalazos6Oswaldo Palenzuela7Ariadna Sitjà-Bobadilla8Jaume Pérez-Sánchez9Fish Pathology Group, Instituto de Acuicultura Torre de la Sal (IATS-CSIC)Nutrigenomics and Fish Growth Endocrinology Group, Instituto de Acuicultura Torre de la Sal (IATS-CSIC)Department of Microbiology and Ecology, Faculty of Biology, University of ValenciaFish Pathology Group, Instituto de Acuicultura Torre de la Sal (IATS-CSIC)Nutrigenomics and Fish Growth Endocrinology Group, Instituto de Acuicultura Torre de la Sal (IATS-CSIC)Norel S.A.BioMar R&DFish Pathology Group, Instituto de Acuicultura Torre de la Sal (IATS-CSIC)Fish Pathology Group, Instituto de Acuicultura Torre de la Sal (IATS-CSIC)Nutrigenomics and Fish Growth Endocrinology Group, Instituto de Acuicultura Torre de la Sal (IATS-CSIC)Abstract Background The 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. Results The 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. Conclusions This 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.http://link.springer.com/article/10.1186/s40168-017-0390-3Sparus aurataIntestinal healthMicrobiomeProteomeSodium butyrateNutrition
spellingShingle María Carla Piazzon
Josep Alvar Calduch-Giner
Belén Fouz
Itziar Estensoro
Paula Simó-Mirabet
Mónica Puyalto
Vasileios Karalazos
Oswaldo Palenzuela
Ariadna Sitjà-Bobadilla
Jaume Pérez-Sánchez
Under control: how a dietary additive can restore the gut microbiome and proteomic profile, and improve disease resilience in a marine teleostean fish fed vegetable diets
Microbiome
Sparus aurata
Intestinal health
Microbiome
Proteome
Sodium butyrate
Nutrition
title Under control: how a dietary additive can restore the gut microbiome and proteomic profile, and improve disease resilience in a marine teleostean fish fed vegetable diets
title_full Under control: how a dietary additive can restore the gut microbiome and proteomic profile, and improve disease resilience in a marine teleostean fish fed vegetable diets
title_fullStr Under control: how a dietary additive can restore the gut microbiome and proteomic profile, and improve disease resilience in a marine teleostean fish fed vegetable diets
title_full_unstemmed Under control: how a dietary additive can restore the gut microbiome and proteomic profile, and improve disease resilience in a marine teleostean fish fed vegetable diets
title_short Under control: how a dietary additive can restore the gut microbiome and proteomic profile, and improve disease resilience in a marine teleostean fish fed vegetable diets
title_sort under control how a dietary additive can restore the gut microbiome and proteomic profile and improve disease resilience in a marine teleostean fish fed vegetable diets
topic Sparus aurata
Intestinal health
Microbiome
Proteome
Sodium butyrate
Nutrition
url http://link.springer.com/article/10.1186/s40168-017-0390-3
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