Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
Regulation of mitochondrial biosynthesis and function by dietary carbohydrate levels and lipid sources in juvenile blunt snout bream Megalobrama amblycephala
Introduction
As two important non-protein energy sources, both carbohydrates and lipids play an important role in regulating the growth performance and metabolism of fish (Zhou et al. 2016). Generally, lipids are regarded as the major non-protein energy-yielding molecule for fish due to their efficient digestion. However, the rich availability and low cost of carbohydrates made their inclusion in diets more attractive (Wilson 1994). The incorporation of this nutrient can not only add beneficial effects to the pelleting quality of feed (Arnesen and Krogdahl 1993) as well as fish growth performance (Peragon et al. 1999), but also can spare protein and lipids in feed as well as reduce the nitrogenous losses of fish into aquatic environment (Hemre and Deng 2015). However, lipids must be considered when maximizing the use of dietary carbohydrates, since lipids and carbohydrates generally have a close relationship with each other in the glycolipid metabolism of fish (Castro et al., 2015, Castro et al., 2016a; Wang et al. 2017). It is thus imperative to determine the interactive effects between dietary carbohydrates and lipids for the species being cultured to facilitate its non-protein energy utilization.
Mitochondria are the major sites of aerobic respiration by cells. In fact, about 90% of the energy is synthesized mainly through the mitochondrial respiratory chain (Eya et al. 2011). Accordingly, both carbohydrates and lipids are oxidized in the mitochondria to generate cellular energy in the form of adenosine triphosphate (ATP). Therefore, mitochondria play an important role in the glycolipid metabolism of animals. Generally, the damage of mitochondrial biosynthesis and function would increase oxidative stress, as could reduce the free radical-scavenging capacity of cells. This could consequently lead to the inhibition of the mitochondrial respiratory chain complex enzymes activities and energy transfer, thereby inhibiting the glycolipid metabolism (Wang et al. 2013). Considering this, maintaining the mitochondrial biosynthesis and function are crucial to promote the non-protein energy utilization by animals.
As a receptor for energy, the adenosine 5′-monophosphate (AMP)-activated protein kinase (AMPK) plays a major role in maintaining the energy balance in cells. The lack of energy would increase the ratio of AMP/ATP, as could consequently activate AMPK, resulting in the increase of catabolism and the inhibition of anabolism. Generally, AMPK is an important activator of peroxisome proliferators γ activated receptor coativator-1 α (PGC-1α), which is the main regulator of mitochondrial biosynthesis, coordinating the function of the body's mitochondrial respiratory chain to meet the supply and demand of different energy (Finck and Kelly 2006). Once activated, AMPK could increase the protein expression of PGC-1α, thereby stimulating the mitochondrial biogenesis and oxidative phosphorylation (Leick et al. 2010). Accordingly, it is generally acknowledged that the AMPK/PGC-1α pathway is one of the most important pathways regulating mitochondrial biosynthesis (Wright et al. 2007). However, to date, this pathway has been mainly investigated in mammals (Ashabi et al. 2014; Leick et al. 2010; Wright et al. 2007). For example, the activation of AMPK by metformin protects against global cerebral ischemia in rats through the mediation of the AMPK/PGC-1α pathway (Ashabi et al. 2014). In addition, thyroid hormone and contractile activity could up-regulate the PGC-1α expression of mouse, thereby inducing mitochondrial adaptations (Irrcher et al. 2003). However, the potential role of this pathway in the mitochondrial biosynthesis of fish is still poorly understood, as warranted further studies.
The function of mitochondrial respiratory chain complex is to produce ATP through a series of redox processes (Eya et al. 2017). Due to its crucial role in energy metabolism, the mitochondrial function of fish has recently drawn considerable attention. To date, the mitochondrial function of fish has been reported to be affected by a large number of factors, such as genetics, growth and/or developmental stages, water temperature, dietary composition, and so on (Houlihan et al. 1993; Papa and Skulachev 1997; Korshunov et al. 1998; Eya et al. 2010). For example, dietary lipid levels have been reported to remarkably affect the liver mitochondrial DNA copy number of large yellow croaker (Larimichthys crocea) (Liao et al. 2016). In addition, the mitochondrial function of rainbow trout (Oncorhynchus mykiss) has been reported to be affected by diets and family (Eya et al. 2011) as well as the interaction between diets and temperature (Eya et al. 2017). However, literatures concerning the nutritional regulations of mitochondrial functions of fish are still quite limited, especially for the interactions between dietary nutrients.
Blunt snout bream Megalobrama amblycephala is an economically important herbivorous freshwater carp in China with a global distribution. In recent years, the need to maximize the profit inevitably leads to a high incorporation of non-protein energy sources in its feed. However, inappropriate use of carbohydrates and lipids might cause metabolic disorders of this species, as consequently results in the increasing outbreaks of fatty liver disease (Prathomya et al. 2017; Prisingkorn et al. 2017). Therefore, it is quite urgent to investigate the non-protein energy utilization by this species, and find an effective approach to promote it. In a previous study, we found that the interactive effects of dietary carbohydrate levels and lipid sources remarkably affected the growth performance and intermediary metabolism of this species (Wang et al. 2017). To further explore the underlying mechanisms, the present study was conducted to evaluate the effects of dietary carbohydrate levels and lipid sources as well as their interaction on the mitochondrial biosynthesis and function of blunt snout bream.
Section snippets
Animal ethics
All experimental procedures involving animals were conducted under the Guidance of the Care and Use of Laboratory Animals in China. The present study was approved by the Animal Care and Use Committee of Nanjing Agricultural University (Nanjing, China) (permit number: SYXK (Su) 2011-0036).
Experimental diets
A 2 × 4 factorial design was used in this study. A total of eight experimental diets were formulated to contain two dietary carbohydrate (namely nitrogen-free extract) levels (30% and 43%) and four lipid
Liver ATP and AMP contents and the AMP/ATP ratio
No statistical difference (P > .05) was observed in liver AMP content (Fig. 1B). The ATP content increased significantly (P < .05) with increasing dietary carbohydrate levels (Fig. 1A), whereas the opposite was true for the AMP/ATP ratio (Fig. 1C). In addition, liver ATP content was significantly (P < .05) affected by dietary lipid sources with the lowest valve obtained in fish fed MO.
The transcriptions of genes involved in the AMPK/PGC-1 pathway
No statistical difference (P > .05) was observed in the transcriptions of PGC-1β among all the treatments (Fig.
Discussion
In previous studies, liver, white muscle and intestine were generally sampled to evaluate the mitochondrial function in fish (Eya et al., 2011, Eya et al., 2015, Eya et al., 2017). In this study, liver was adopted as the target organ to investigate the effects of dietary non-protein energy levels and/or sources on the mitochondrial biosynthesis and function of blunt snout bream. This is due to the fact that liver is the center of intermediary metabolism, and that mitochondria in hepatocytes are
Acknowledgements
This research was funded by the National Natural Science Foundation of China (31872576) and the National Technology System of Conventional Freshwater Fish Industries in China (CARS-45-14).
References (80)
Adenosine-5′-diphosphate and Adenosine-5′-monophosphate
Meth. Enzymatic Anal.
(1965)- et al.
Crude and pre-extruded products of wheat as nutrient sources in extruded diets for Atlantic salmon (Salmo salar L.) grown in sea water
Aquaculture
(1993) - et al.
Failure of ATP supply to match ATP demand: the mechanism of toxicity of the lampricide, 3-trifluoromethyl-4-nitrophenol (TFM), used to control sea lamprey (Petromyzon marinus) populations in the Great Lakes
Aquat. Toxicol.
(2009) - et al.
Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues
Methods Cell Biol.
(2001) - et al.
The oxidation of ubiquinol by the isolated rieske iron-sulfur protein in solution
Arch. Biochem. Biophys.
(1990) - et al.
A long-term high-fat diet increases oxidative stress, mitochondrial damage and apoptosis in the inner ear of D-galactose-induced aging rats
Hear. Res.
(2012) - et al.
Association of mitochondrial function with feed efficiency in rainbow trout: Diets and family effects
Aquaculture
(2011) - et al.
Genetic variation in feed consumption, growth, nutrient utilization efficiency and mitochondrial function within a farmed population of channel catfish (Ictalurus punctatus)
Comp. Biochem. Physiol. B
(2012) - et al.
Combined effects of diets and temperature on mitochondrial function, growth and nutrient efficiency in rainbow trout (Oncorhynchus mykiss)
Comp. Biochem. Physiol. B
(2017) - et al.
Differential investigation of the capacity of succinate oxidation in human skeletal muscle
Clin. Chim. Acta
(1985)
Effects of dietary oxidized fish oil with vitamin E supplementation on growth performance and reduction of lipid peroxidation in tissues and blood of Red sea bream Pagrosomus major
Aquaculture
Biochemical assays of respiratory chain complex activity
Methods Cell Biol.
Fatty acids as nuatral uncouplers preventing generation of O2 and H2O2 by mitochondria in the resting state
FEBS Lett.
Effects of different dietary soybean oil levels on growth, lipid deposition, tissues fatty acid composition and hepatic lipid metabolism related gene expressions in blunt snout bream (Megalobrama amblycephala) juvenile
Aquaculture
Effect of dietary fatty acids on lipoprotein lipase gene expression in the liver and visceral adipose tissue of fed and starved red sea bream Pagrus major
Comp. Biochem. Physiol. A
Dietary lipid concentration affects liver mitochondrial dna copy number, gene expression and dna methylation in large yellow croaker (Larimichthys crocea)
Comp. Biochem. Physiol. B
Analysis of relative gene expression data using realtime quantitative PCR and the 2- ΔΔCt method
Methods
Protein measurement with the folin phenol reagent
J. Biol. Chem.
Carbohydrates affect protein-turnover rates, growth, and nucleic acid content in the white muscle of rainbow trout (Oncorhynchus mykiss)
Aquaculture
A simplification of the protein assay method of Lowry et al. which is more generally applicable
Anal. Biochem.
The AMP-regulated kinase family: enigmatic targets for diabetes therapy
Mol. Cell. Endocrinol.
Nervonic acid versus, tricosanoic acid as internal standards in quantitative gas chromatographic analyses of fish oil longer-chain n-3 polyunsaturated fatty acid methyl esters
J. Chromatogr. A
Dietary carbohydrate levels and lipid sources modulate the growth performance, fatty acid profiles and intermediary metabolism of blunt snout bream Megalobrama amblycephala in an interactive pattern
Aquaculture
Utilization of dietary carbohydrate by fish
Aquaculture
Exercise-induced mitochondrial biogenesis begins before the increase in muscle pgc-1α expression
J. Biol. Chem.
Interactions between dietary carbohydrate and metformin: implications on energy sensing, insulin signaling pathway, glycolipid metabolism and glucose tolerance in blunt snout bream megalobrama amblycephala
Aquaculture
Sequence analysis and expression differentiation of chemokine receptor CXCR4b among three populations of Megalobrama amblycephala
Dev. Comp. Immunol.
Effects of dietary carbohydrate to lipid ratios on growth performance, digestive enzyme and hepatic carbohydrate metabolic enzyme activities of large yellow croaker (Larmichthys crocea)
Aquaculture
Agricultural chemicals; contaminants, drugs
Activation of amp-activated protein kinase by metformin protects against global cerebral ischemia in male rats: interference of AMPK/PGC-1α pathway
Metab. Brain Dis.
Methods of Enzymatic Analysis
Control of glycogen synthase trough adipor-1-ampk pathway in renal distal tubules of normal and diabetic rats
Am. J. Physiol. Ren. Physiol.
Dietary carbohydrate and lipid source affect cholesterol metabolism of European sea bass (Dicentrarchus labrax) juveniles
Br. J. Nutr.
Regulation of glucose and lipid metabolism by dietary carbohydrate levels and lipid sources in gilthead sea bream juveniles
Br. J. Nutr.
Dietary lipid and carbohydrate interactions: implications on lipid and glucose absorption, transport in gilthead sea bream (Sparus aurata) juveniles
Lipids
ATP levels and adenylate energy charge in soils of mangroves in the Andamans
Curr. Sci.
Influence of diet on mitochondrial complex activity in channel catfish, Ictalurus punctatus
N. Am. J. Aquac.
Interactive effects of dietary lipid and phenotypic feed efficiency on the expression of nuclear and mitochondrial genes involved in the mitochondrial electron transport chain in rainbow trout
Int. J. Mol. Sci.
PGC-1 coactivators: inducible regulators of energy metabolism in health and disease
J. Cin. Invest.
Transcriptome analysis and SSR/SNP markers information of the blunt snout bream (Megalobrama amblycephala)
PLoS One
Cited by (9)
A time-course study of the effects of a high-carbohydrate diet on the growth performance, glycolipid metabolism and mitochondrial biogenesis and function of blunt snout bream (Megalobrama amblycephala)
2022, AquacultureCitation Excerpt :Recently, PGC-1β has been demonstrated to be more effective in inducing mitochondrial biogenesis in fish than PGC-1α (Bremer et al., 2016; Lu et al., 2020). In addition, the poor carbohydrate utilization by fish has been partially linked to mitochondrial dysfunctions (Xu et al., 2018; Li et al., 2019). However, how high-carbohydrate diets induce mitochondrial dysfunctions and glucose metabolism disorders in fish is still not fully unveiled, and warrants further studies.
Carbonyl cyanide 3-chlorophenylhydrazone induced the imbalance of mitochondrial homeostasis in the liver of Megalobrama amblycephala: A dynamic study
2021, Comparative Biochemistry and Physiology Part - C: Toxicology and PharmacologyCitation Excerpt :Furthermore, high-fat diets can activate the mitochondrial biogenesis, fusion and oxidation, thereby reducing the lipid accumulation mediated in yellow catfish (Pelteobagrus fulvidraco) (Song et al., 2020). Nonetheless, high dietary carbohydrate levels significantly depressed the mitochondrial fusion, mitochondrial biogenesis and mitochondrial oxidative phosphorylation capability of blunt snout bream (Megalobrama amblycephala) while enhancing mitochondrial fission (Li et al., 2019; Xu et al., 2018). However, to date, the potential mechanisms underlying these physiological processes are still poorly understood.
Utilization of raw and gelatinized starch by blunt snout bream Megalobrama amblycephala as evidenced by the glycolipid metabolism, glucose tolerance and mitochondrial function
2020, AquacultureCitation Excerpt :Further, transcription of the mitochondrial respiratory chain related genes were affected by varying dietary fat levels and resulting feed efficiency values in rainbow trout (Oncorhynchus mykiss) (Eya et al., 2015). Intermediary metabolism and mitochondrial biogenesis and function in blunt snout bream Megalobrama amblycephala were signicantly affected by dietary carbohydrate concentrations, lipid sources and their interaction (Wang et al., 2017a, 2017b; Li et al., 2019). However, it is not clear whether the degree of starch gelatinization affects the mitochondrial function of fish.