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

Type Article
Date 2016-11
Language English
Author(s) Gatesoupe Francois-Joel1, 3, Huelvan Christine2, Le Bayon Nicolas2, Le Delliou Herve2, Madec Lauriane2, Mouchel OlivierORCID2, Quazuguel PatrickORCID2, Mazurais DavidORCID2, Zambonino-Infante Jose-LuisORCID2
Affiliation(s) 1 : Univ Pau & Pays Adour, INRA, NUMEA, F-64310 St Pee Sur Nivelle, France.
2 : IFREMER, PFOM ARN, Ctr Bretagne, UMR LEMAR 6539, CS 10070, F-29280 Plouzane, France.
3 : IFREMER, PFOM ARN, Ctr Bretagne, CS 10070, F-29280 Plouzane, France.
Source Bmc Microbiology (1471-2180) (Biomed Central Ltd), 2016-11 , Vol. 16 , N. 266 , P. 1-13
DOI 10.1186/s12866-016-0885-2
WOS© Times Cited 46
Keyword(s) Host-microbe interaction, 16S rRNA, Pyrosequencing, Autochthonous bacteria, Alternative feed ingredients, Physiological status
Abstract 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.
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Publisher's official version 13 794 KB Open access
Additional file 1: Rarefaction curves of OTU richness of each sample from the experimental groups, computed after normalization to 11599 reads per sample. 916 KB Open access
Additional file 2: Venn diagram showing the distribution of the 1111 OTUs among the intestinal samples of the five experimental groups. 233 KB Open access
Additional file 3: Histogram showing the overwhelming dominance of Alpha- and Gamma-Proteobacteria among the OTUs detected in every experimental group. 63 KB Open access
Additional file 4: Histogram showing the distribution of the most dominant OTUs (more than 5 % total reads in at least one sample). 2 MB Open access
Additional file 5: Mean relative abundance of phylogenetic clusters among Gammaproteobacteria with significant differences between experimental groups. 1 294 KB Open access
Additional file 6: Mean relative abundance of phylogenetic clusters among Alpha- and Beta-Proteobacteria with significant differences between experimental groups. 1 273 KB Open access
Additional file 7: Mean relative abundance of phylogenetic clusters among Actinobacteria and Firmicutes with significant differences between experimental groups. 1 274 KB Open access
Additional file 8: Mean relative abundance of phylogenetic clusters among Bacteroidetes and Spirochaetae with significant differences between experimental groups. 1 283 KB Open access
Additional file 9: Mean weights (± SE) of sea bass before, at midterm, and after the final dietary challenge of sea bass. 1 87 KB Open access
Additional file 10: Hypoxia resistance time (h) of the individuals selected for the microbiological analysis. 1 209 KB Open access
Additional file 11: Phylogenetic tree derived by neighbour joining of the three Bacillus sp. OTUs from the present intestinal samples, aligned with GenBank sequences. 64 KB Open access
Additional file 12: Sequences of the primers used in the nested PCR for pyrosequencing. 1 85 KB Open access
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How to cite 

Gatesoupe Francois-Joel, Huelvan Christine, Le Bayon Nicolas, Le Delliou Herve, Madec Lauriane, Mouchel Olivier, Quazuguel Patrick, Mazurais David, Zambonino-Infante Jose-Luis (2016). The highly variable microbiota associated to intestinal mucosa correlates with growth and hypoxia resistance of sea bass, Dicentrarchus labrax, submitted to different nutritional histories. Bmc Microbiology, 16(266), 1-13. Publisher's official version : https://doi.org/10.1186/s12866-016-0885-2 , Open Access version : https://archimer.ifremer.fr/doc/00356/46719/