Transcriptomics, metabolomics and histology indicate that high-carbohydrate diet negatively affects the liver health of blunt snout bream (Megalobrama amblycephala)

Wassana Prisingkorn,Ivan Jakovlić,Panita Prathomya,Wei-Min Wang,Han Liu,Yu-Hua Zhao

doi:10.1186/s12864-017-4246-9

Wassana Prisingkorn, Ivan Jakovlić + Show 4 more

Open Access

https://doi.org/10.1186/s12864-017-4246-9

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Abstract

BackgroundGlobal trend of the introduction of high levels of relatively cheap carbohydrates to reduce the amount of costly protein in the aquatic animal feed production has affected the aquaculture of an economically important cyprinid fish, blunt snout bream (Megalobrama amblycephala). This dietary shift has resulted in increased prevalence of metabolic disorders, often causing economic losses. High dietary intake of carbohydrates, associated with obesity, is one of the major causes of non-alcoholic fatty liver disease (NAFLD) in humans.ResultsWe have conducted an eight-week feeding trial to better understand how a high-carbohydrate diet (HCBD) affects the liver health in this fish. Hepatosomatic index and lipid content were significantly (P < 0.05) higher in the HCBD group. Histology results also suggested pathological changes in the livers of HCBD group, with excessive lipid accumulation and indication of liver damage. Metabolomics and serum biochemistry analyses showed that a number of metabolites indicative of liver damage were increased in the HCBD group. This group also exhibited low levels of betaine, which is a metabolite crucial for maintaining the healthy liver functions. Transcriptomic and qPCR analyses indicated that HCBD had a strong impact on the expression of a large number of genes associated with the NAFLD and insulin signalling pathways, which may lead to the development of insulin resistance in hepatocytes, pathological liver changes, and eventually the NAFLD.ConclusionsTranscriptomics, metabolomics and histology results all indicate early symptoms of liver damage. However whether these would actually lead to the development of NAFLD after a longer period of time, remains inconclusive. Additionally, a very high number of upregulated genes in the HCBD group associated with several neurodegenerative diseases is a strong indication of neurodegenerative changes caused by the high-carbohydrate diet in blunt snout bream. This suggests that fish might present a good model to study neurodegenerative changes associated with high-carbohydrate diet in humans.

Highlights

Global trend of the introduction of high levels of relatively cheap carbohydrates to reduce the amount of costly protein in the aquatic animal feed production has affected the aquaculture of an economically important cyprinid fish, blunt snout bream (Megalobrama amblycephala)
Liver lipid content and histology analyses have revealed the cause for the significant difference in the two hepatosomatic index (HSI) values: the control group had regular hepatocytes with large and spherical nuclei centrally located in a moderate cytoplasm and a small number of lipid droplets (Fig. 1a, c); in contrast, the high-carbohydrate diet (HCBD) group exhibited swollen hepatocytes with large diffused lipid vacuoles, abnormal endothelial cells in the central liver vein, inflammatory infiltrate and some hypertrophy of the hepatocytes (Fig. 1b, d)
Our metabolomics results show that the high dietary carbohydrate intake induced significant increases in plasma α/β-glucose, succinate and tyrosine (Fig. 2), all of which can be converted to acetyl-CoA in the tricarboxylic acid (TCA) cycle pathway, which connects the glucose metabolism with the fatty acid metabolism

Summary

Introduction

Global trend of the introduction of high levels of relatively cheap carbohydrates to reduce the amount of costly protein in the aquatic animal feed production has affected the aquaculture of an economically important cyprinid fish, blunt snout bream (Megalobrama amblycephala). This dietary shift has resulted in increased prevalence of metabolic disorders, often causing economic losses. High dietary intake of carbohydrates, associated with obesity, is one of the major causes of non-alcoholic fatty liver disease (NAFLD) in humans. High dietary intake of carbohydrates has been associated with increased risks of obesity in fish, and zebrafish and medaka were used as models to investigate whether fish livers are affected by excessive dietary carbohydrates, including changes in liver size, cellular architecture, gene expression patterns, and lipid accumulation, the correlation between high carbohydrate diet and NAFLD in fish remains inconclusive [16,17,18]

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