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The highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, Dicentrarchus labrax, submitted to different nutritional histories

BACKGROUND: The better understanding of how intestinal microbiota interacts with fish health is one of the key to sustainable aquaculture development. The present experiment aimed at correlating active microbiota associated to intestinal mucosa with Specific Growth Rate (SGR) and Hypoxia Resistance...

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Autores principales: Gatesoupe, François-Joël, Huelvan, Christine, Le Bayon, Nicolas, Le Delliou, Hervé, Madec, Lauriane, Mouchel, Olivier, Quazuguel, Patrick, Mazurais, David, Zambonino-Infante, José-Luis
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100225/
https://www.ncbi.nlm.nih.gov/pubmed/27821062
http://dx.doi.org/10.1186/s12866-016-0885-2
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author Gatesoupe, François-Joël
Huelvan, Christine
Le Bayon, Nicolas
Le Delliou, Hervé
Madec, Lauriane
Mouchel, Olivier
Quazuguel, Patrick
Mazurais, David
Zambonino-Infante, José-Luis
author_facet Gatesoupe, François-Joël
Huelvan, Christine
Le Bayon, Nicolas
Le Delliou, Hervé
Madec, Lauriane
Mouchel, Olivier
Quazuguel, Patrick
Mazurais, David
Zambonino-Infante, José-Luis
author_sort Gatesoupe, François-Joël
collection PubMed
description BACKGROUND: The better understanding of how intestinal microbiota interacts with fish health is one of the key to sustainable aquaculture development. The present experiment aimed at correlating active microbiota associated to intestinal mucosa with Specific Growth Rate (SGR) and Hypoxia Resistance Time (HRT) in European sea bass individuals submitted to different nutritional histories: the fish were fed either standard or unbalanced diets at first feeding, and then mixed before repeating the dietary challenge in a common garden approach at the juvenile stage. RESULTS: A diet deficient in essential fatty acids (LH) lowered both SGR and HRT in sea bass, especially when the deficiency was already applied at first feeding. A protein-deficient diet with high starch supply (HG) reduced SGR to a lesser extent than LH, but it did not affect HRT. In overall average, 94 % of pyrosequencing reads corresponded to Proteobacteria, and the differences in Operational Taxonomy Units (OTUs) composition were mildly significant between experimental groups, mainly due to high individual variability. The highest and the lowest Bray-Curtis indices of intra-group similarity were observed in the two groups fed standard starter diet, and then mixed before the final dietary challenge with fish already exposed to the nutritional deficiency at first feeding (0.60 and 0.42 with diets HG and LH, respectively). Most noticeably, the median percentage of Escherichia-Shigella OTU_1 was less in the group LH with standard starter diet. Disregarding the nutritional history of each individual, strong correlation appeared between (1) OTU richness and SGR, and (2) dominance index and HRT. The two physiological traits correlated also with the relative abundance of distinct OTUs (positive correlations: Pseudomonas sp. OTU_3 and Herbaspirillum sp. OTU_10 with SGR, Paracoccus sp. OTU_4 and Vibrio sp. OTU_7 with HRT; negative correlation: Rhizobium sp. OTU_9 with HRT). CONCLUSIONS: In sea bass, gut microbiota characteristics and physiological traits of individuals are linked together, interfering with nutritional history, and resulting in high variability among individual microbiota. Many samples and tank replicates seem necessary to further investigate the effect of experimental treatments on gut microbiota composition, and to test the hypothesis whether microbiotypes may be delineated in fish. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-016-0885-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-51002252016-11-08 The highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, Dicentrarchus labrax, submitted to different nutritional histories Gatesoupe, François-Joël Huelvan, Christine Le Bayon, Nicolas Le Delliou, Hervé Madec, Lauriane Mouchel, Olivier Quazuguel, Patrick Mazurais, David Zambonino-Infante, José-Luis BMC Microbiol Research Article BACKGROUND: The better understanding of how intestinal microbiota interacts with fish health is one of the key to sustainable aquaculture development. The present experiment aimed at correlating active microbiota associated to intestinal mucosa with Specific Growth Rate (SGR) and Hypoxia Resistance Time (HRT) in European sea bass individuals submitted to different nutritional histories: the fish were fed either standard or unbalanced diets at first feeding, and then mixed before repeating the dietary challenge in a common garden approach at the juvenile stage. RESULTS: A diet deficient in essential fatty acids (LH) lowered both SGR and HRT in sea bass, especially when the deficiency was already applied at first feeding. A protein-deficient diet with high starch supply (HG) reduced SGR to a lesser extent than LH, but it did not affect HRT. In overall average, 94 % of pyrosequencing reads corresponded to Proteobacteria, and the differences in Operational Taxonomy Units (OTUs) composition were mildly significant between experimental groups, mainly due to high individual variability. The highest and the lowest Bray-Curtis indices of intra-group similarity were observed in the two groups fed standard starter diet, and then mixed before the final dietary challenge with fish already exposed to the nutritional deficiency at first feeding (0.60 and 0.42 with diets HG and LH, respectively). Most noticeably, the median percentage of Escherichia-Shigella OTU_1 was less in the group LH with standard starter diet. Disregarding the nutritional history of each individual, strong correlation appeared between (1) OTU richness and SGR, and (2) dominance index and HRT. The two physiological traits correlated also with the relative abundance of distinct OTUs (positive correlations: Pseudomonas sp. OTU_3 and Herbaspirillum sp. OTU_10 with SGR, Paracoccus sp. OTU_4 and Vibrio sp. OTU_7 with HRT; negative correlation: Rhizobium sp. OTU_9 with HRT). CONCLUSIONS: In sea bass, gut microbiota characteristics and physiological traits of individuals are linked together, interfering with nutritional history, and resulting in high variability among individual microbiota. Many samples and tank replicates seem necessary to further investigate the effect of experimental treatments on gut microbiota composition, and to test the hypothesis whether microbiotypes may be delineated in fish. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12866-016-0885-2) contains supplementary material, which is available to authorized users. BioMed Central 2016-11-08 /pmc/articles/PMC5100225/ /pubmed/27821062 http://dx.doi.org/10.1186/s12866-016-0885-2 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Gatesoupe, François-Joël
Huelvan, Christine
Le Bayon, Nicolas
Le Delliou, Hervé
Madec, Lauriane
Mouchel, Olivier
Quazuguel, Patrick
Mazurais, David
Zambonino-Infante, José-Luis
The highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, Dicentrarchus labrax, submitted to different nutritional histories
title The highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, Dicentrarchus labrax, submitted to different nutritional histories
title_full The highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, Dicentrarchus labrax, submitted to different nutritional histories
title_fullStr The highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, Dicentrarchus labrax, submitted to different nutritional histories
title_full_unstemmed The highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, Dicentrarchus labrax, submitted to different nutritional histories
title_short The highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, Dicentrarchus labrax, submitted to different nutritional histories
title_sort highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, dicentrarchus labrax, submitted to different nutritional histories
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100225/
https://www.ncbi.nlm.nih.gov/pubmed/27821062
http://dx.doi.org/10.1186/s12866-016-0885-2
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