Dataset Information

Gut segments outweigh the diet in shaping the intestinal microbiota composition in grass carp Ctenopharyngodon idellus.

ABSTRACT: Although dynamics of the complex microbial ecosystem populating the gastrointestinal tract of animals has profound and multifaceted impacts on host's metabolism and health, it remains unclear whether it is the intrinsic or extrinsic factors that play a more dominant role in mediating the composition of intestinal microbiota. To address this, we studied the impacts of two strikingly different diets on a herbivorous fish, grass carp (Ctenopharyngodon idellus): a high-protein, low-fiber formula feed, and low-protein, high-fiber Sudan grass. After a 16-week feeding trial, microbial profiles of midgut and hindgut segments in both groups were compared. Bacterial composition was significantly different between the midguts of both groups, but not between the hindguts of two groups. Both PerMANOVA and VPA analyses suggested that gut segments explain a higher proportion of variation in intestinal microbiota than diet. Overall, our results suggest that intestinal compartments are a stronger determinant than diet in shaping the intestinal microbiota. Specifically, whereas diet has a strong impact on the composition of microbiota in proximal gut compartments, this impact is much less pronounced distally, which is likely to be a reflection of a limited ability of some microbial taxa to thrive in the anoxic environment in distal segments.

SUBMITTER: Feng W

PROVIDER: S-EPMC6451743 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Gut segments outweigh the diet in shaping the intestinal microbiota composition in grass carp Ctenopharyngodon idellus.

Feng Wenwen W Zhang Jing J Jakovlić Ivan I Xiong Fan F Wu Shangong S Zou Hong H Li Wenxiang W Li Ming M Wang Guitang G

AMB Express 20190406 1

Although dynamics of the complex microbial ecosystem populating the gastrointestinal tract of animals has profound and multifaceted impacts on host's metabolism and health, it remains unclear whether it is the intrinsic or extrinsic factors that play a more dominant role in mediating the composition of intestinal microbiota. To address this, we studied the impacts of two strikingly different diets on a herbivorous fish, grass carp (Ctenopharyngodon idellus): a high-protein, low-fiber formula fee ...[more]

PMID: 30955112

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Project description:BackgroundThe ultrahigh density intensive farming model of grass carp (Ctenopharyngodon idellus) may elicit growth inhibition, decrease flesh quality, and increase disease susceptibility of fish. The degradation in quality and excessive fat accumulation in cultured C. idellus have long been attributed to possible alterations in the lipid metabolism of fish muscle tissues as a result of overnutrition from artificial diets. To investigate the effects of different diets on fish muscle quality, a large-scale metabolomics study was performed on 250 tails of C. idellus.FindingsThe experimental fish were divided into four groups based on sex and diet-female artificial feed (FAF), female grass feed, male artificial feed (MAF), and male grass feed (MGF). After a 113-day rearing period, the artificial feed (AF) group showed a significantly higher total mass of muscle fat (P < 0.01), with the FAF group being the highest. Metabolomics profiling based on liquid chromatography-mass spectrometry revealed distinctive patterns of clustering according to the four groups. Overall, artificial feeding was associated with higher concentrations of docosapentaenoic acid, dihomo-gamma-linolenic acid, and arachidonic acid, whereas grass feeding was associated with elevated n-3 unsaturated fatty acids (UFAs) such as eicosapentaenoic acid, alpha-linolenic acid, and gamma-linolenic acid. Artificial feeding also resulted in significant increased docosahexaenoic acid in MAF muscle than in MGF fish, whereas there was no significance in the comparison of female samples. Metabolic pathway analyses using both targeted and untargeted approaches consistently revealed that arachidonic acid metabolism and steroid hormone biosynthesis pathways were significantly different between AF and grass fed groups.ConclusionsOur results suggest that grass is a better source of dietary fatty acid and protein when compared to artificial feed. Grass feeding could effectively lower triglycerides in serum, reduce fat accumulation, and alter lipid compositions in fish muscle by increasing the concentrations of n-3 UFAs, leading to better nutrition and health.

Project description:Grass carp (Ctenopharyngodon idellus; n = 320) were received four different diets for 56 days. The experimental diets were: fishmeal (FM) containing 10% fishmeal (without rapeseed meal), and rapeseed meal (RM) containing 50% rapeseed meal (without fishmeal), and two semi-purified diets either without (T0) or with 1.25% (T1) supplemental hydrolysable tannin. The approximate content of tannin in the RM diet was 1.31%, which was close to that of T1, while the tannin content of FM was close to that of T0. The weight gain rate of grass carp of the RM group was significantly lower than that of the FM group, while the feeding conversion ratio and the feeding rate were significantly higher in the T1 group than in T0. The muscle lipid content was significantly lower in RM than in FM, while T1 was lower than T0. Intestinal activities of trypsin and α-amylase were significantly higher in T1 and RM groups compared with the other treatments. The hepatic activities of aspartate aminotransferase and alanine aminotransferase were lower in T1 and RM groups compared with the other treatments, while hepatic glycogen, and malonaldehyde were significantly higher in T1 and RM groups. In serum, the total protein and globulin contents were significantly higher in T1 and RM groups, while albumin was significantly lower in the RM group compared to the FM group. High-throughput sequencing showed that Proteobacteria, Firmicutes, and Actinobacteria were the dominant bacterial phyla among groups. The intestinal microbial diversity was higher in T1 and RM. Redundancy analysis showed that tannin, rapeseed meal, and intestinal trypsin activity were positively or negatively correlated with the relative abundance of several different intestinal microbiota at phylum and/or genus levels. The results indicated that 1.25% tannin could not be the main reason for the poor growth of grass carp of the RM group; however, the protein metabolism was disturbed, the absorption of carbohydrate was improved, and the accumulation of lipid had decreased. Furthermore, tannin and rapeseed meal supplementations modulated the intestinal microbiota, and may sequentially regulate the intestinal function by fermenting dietary nutrition, producing digestive enzymes, and modulating probiotics.

Project description:The present study explored the effects of ferulic acid (FA) supplementation in cottonseed meal (CSM)-based diets on grass carp growth performance, feed utilization, liver antioxidation status, and intestinal physical barrier function. Here, four experimental diets supplemented with FA at graded levels (0, 50, 100 and 200 mg/kg) and CSM as the main protein source (384.6 g/kg feed) for an 8-week feeding trial. Our results indicated that 200 mg/kg FA supplementation in a CSM-based diet significantly improved growth performance [including final body weight (FBW), weight gain rate, and specific growth rate] and feed utilization [including feed conversion ratio and protein efficiency ratio] in grass carp (p < 0.05). The results of polynomial regression analysis based on FBW recommended that the optimal dose for FA supplementation was 204 mg/kg. Compared with that no FA supplementation, 200 mg/kg FA supplementation significantly reduced liver malondialdehyde levels and increased glutathione reductase activities (p < 0.05) and 100 mg/kg FA supplementation significantly increased liver total superoxide dismutase activities and reduced blood alanine transaminase levels (p < 0.05). Compared with the control group, 100 mg/kg FA supplementation also led to significantly increased mRNA expression of zo-1, zo-2, occludin, claudin-b, claudin-3, claudin-7a, and claudin-12, encoding intestinal tight junction proteins (p < 0.05). Notably, FA supplementation could reduce lipid deposition by regulating bile acid (BA) secretion. In this study, 100 and 200 mg/kg FA supplementation significantly increased blood and liver total BA levels, respectively (p < 0.05); 100 mg/kg FA also significantly activated mRNA expressions of fxr and cyp7a1 (p < 0.05). Furthermore, the whole-body composition results presented that FA treatment relieved lipid deposition, particularly 50 and 200 mg/kg FA supplementation (p < 0.05). Moreover, triglyceride and total cholesterol levels were significantly lower and high-density lipoprotein levels were significantly higher with 200 mg/kg FA supplementation than with no FA supplementation (p < 0.05). Taken together, the results indicated that FA may be a beneficial feed additive to boost fish growth performance and increase CSM utilization.

Dataset Information

Gut segments outweigh the diet in shaping the intestinal microbiota composition in grass carp Ctenopharyngodon idellus.

Publications

Gut segments outweigh the diet in shaping the intestinal microbiota composition in grass carp Ctenopharyngodon idellus.

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