Home Journals Articles Updates About
CN
image
收藏切换
Effect of dietary supplementation of selenium-L-methionine on growth, antioxidant capacity and resistance to nitrite stress of spotted seabass (Lateolabrax maculatus) under two rearing water temperatures
收藏切换
PDF
Xiao Li, Jing Li, Kangle Lu, Xueshan Li, Kai Song, Ling Wang*, Chunxiao Zhang
Animal Nutrition | 2024, 19(1) : 166 - 179
Less
收藏切换
Animal Nutrition | 2024, 19(1): 166-179
• Original Research Article •
Effect of dietary supplementation of selenium-L-methionine on growth, antioxidant capacity and resistance to nitrite stress of spotted seabass (Lateolabrax maculatus) under two rearing water temperatures
Full
Xiao Li, Jing Li, Kangle Lu, Xueshan Li, Kai Song, Ling Wang*, Chunxiao Zhang
Affiliations
  • Xiamen Key Laboratory for Feed Quality Testing and Safety Evaluation, Fisheries College, Jimei University, Xiamen 361021, China
Published: 2024-12-10 doi: 10.1016/j.aninu.2023.12.013
Outline
收藏切换

A 10-week feeding trial, followed by 24-h nitrite stress, was performed to evaluate the effects of dietary selenium-L-methionine (Se-Met) on growth, Se accumulation, antioxidant capacity, transcripts of selenoproteins and histological changes of muscle as well as resistance to nitrite stress in spotted seabass (Lateolabrax maculatus) reared at optimal (27℃) and high (33℃) temperatures. Five experimental diets were formulated to contain Se-Met at 0, 0.9, 1.8, 3.5, and 7.0 mg/kg. Each diet was fed to fish (2.60 ± 0.2 g) in two parallel treatments at 27 or 33℃. The results showed that elevated temperature (33℃) induced thermal stress in fish, and fish under thermal stress exhibited lower weight gain and hepatosomatic index but a higher condition factor compared to those reared at 27℃. However, the growth and feed utilisation were promoted in L. maculatus with 0.9 to 3.5 mg/kg Se-Met treatments. The protein and lipid content in the muscle increased with the dietary Se-Met level, and the total Se level in the whole body and muscle showed a linear increase with dietary Se-Met supplementation. Thermal stress changed the histology of the muscle, leading to raised levels of malondialdehyde (MDA), reduced antioxidant parameters in the serum and liver, and a decrease in the transcripts of selenoprotein genes in the muscle. Meanwhile, increased antioxidant capacity of serum and liver and up-regulated transcripts of selenoprotein of muscle were observed in L. maculatus reaching a maximum with 3.5 mg Se-Met/kg treatment. After 24 h of nitrite stress, thermal stress exacerbated oxidative damage caused by nitrite stress in L. maculatus. In contrast, dietary Se-Met enhanced the resistance to nitrite stress of L. maculatus fed with Se-Met enriched diets containing 0.9 to 1.8 mg Se-Met/kg. Based on the effects of dietary Se-Met on the growth, antioxidant capacity and resistance to nitrite stress of L. maculatus, this study suggests that the optimal range of Se-Met supplementation in L. maculatus diets is 1.80 to 2.39 mg Se-Met/kg of diet at 27℃ and 1.80 to 4.46 mg Se-Met/kg of diet at 33℃.

Lateolabrax maculatus  /  Elevated temperature  /  Selenium-L-methionine  /  Growth  /  Antioxidant capacity  /  Nitrite stress
Xiao Li, Jing Li, Kangle Lu, Xueshan Li, Kai Song, Ling Wang, Chunxiao Zhang. Effect of dietary supplementation of selenium-L-methionine on growth, antioxidant capacity and resistance to nitrite stress of spotted seabass (Lateolabrax maculatus) under two rearing water temperatures[J]. Animal Nutrition, 2024 , 19 (1) : 166 -179 . DOI: 10.1016/j.aninu.2023.12.013
Full Text
Less
1.　Introduction
Less
Water temperature is one of the most pervasive and influential environmental factors in intensive aquaculture, which directly impacts nearly all aspects of fish physiology (Buentello et al., 2000; Zak and Manzon, 2019). Maintaining an optimal water temperature range is crucial for ensuring the normal growth, feed utilization, physiological metabolism, and survival of fish (Bansemer et al., 2018; Buentello et al., 2000). However, water temperatures in outdoor aquaculture fluctuate with seasons, often deviating from the optimal range for cultured fish (Zeng et al., 2021). In summer, the impact of elevated temperatures on aquaculture fish cannot be avoided. In a short-term high-temperature environment, fish maintain relative body temperature balance mainly through regulating various hormones (i.e., thyroxine) (Zak and Manzon, 2019). However, chronically elevated water temperature-induced thermal stress can have various negative effects on fish growth, physiology and survival (Kim et al., 2016; Matthews and Berg, 1997; Vinagre et al., 2012), with oxidative stress caused by excess reactive oxygen species (ROS) being one of the main reasons for these adverse responses in fish (Cheng et al., 2018; Kim et al., 2017). In general, adding an appropriate proportion of antioxidants into fish feed is a practical and effective way to prevent or mitigate oxidative stress caused by thermal temperature (Li et al., 2023; Yuan et al., 2023). Thus, it is important to explore the interactions between fish nutritional requirements for antioxidants and water temperature to achieve maximum growth potential.
In aquatic organisms, selenium (Se) is an effective exogenous antioxidant which plays a role in the removal of reactive oxygen species and preventing oxidative stress caused by changes in environmental factors (Li et al., 2022; Wang et al., 2019, 2021a). Meanwhile, Se plays a crucial role in maintaining normal growth and physiological functions in fish (Gatlin and Wilson, 1984; Schrauzer, 2000) and is toxic in excess (Janz et al., 2010). In general, Se forms supplemented in feed mainly include sodium selenite and organic Se, i.e., selenium-L-methionine (Se-Met) and Se-yeast (Ghaniem et al., 2022; Liu et al., 2017). Early studies on dietary Se mainly focused on evaluating the optimal requirement of inorganic Se (Gatlin and Wilson, 1984). However, Se-Met is the dominant organic Se form (>80%) found in organisms, with higher bioavailability than inorganic Se and is more readily assimilated and accumulated in fish (Wang and Lovell, 1997). Some studies have demonstrated that several fish species exhibit greater weight gain and feed utilisation when fed diets supplemented with organic Se as opposed to inorganic Se (when total Se levels are comparable) (Lin, 2014; Liu et al., 2017; Wang et al., 2007). Thus, a lower amount of dietary Se supplementation is expected to achieve similar effects on growth with the replacement of inorganic Se with Se-Met (Liu et al., 2017; Wang and Lovell, 1997). Overall, it is necessary to revise or evaluate the optimal level of supplementation of Se for fish species commonly used in aquaculture when Se is added to fish diets in the form of Se-Met.
Se exerts its diverse biological functions by participating in the synthesis of 41 selenoproteins in the teleost (Mariotti et al., 2012). These selenoprotein families involved in thermal stress regulation primarily include regulation of the redox homeostasis by glutathione peroxidase (GPx) and thioredoxin reductase (TXNRD), as well as synthesis and metabolism of thyroxine by iodothyronine deiodinase (DIO) in organisms (Drigo et al., 2013; Weekley and Harris, 2013). Although the functions of Se-Met in improving growth, Se accumulation, feed conversion, antioxidant capacity, immunity and flesh quality in fish have been investigated (Chen et al., 2020; Lin, 2014; Liu et al., 2017; Mechlaoui et al., 2019; Rider et al., 2009; Wang et al., 2021b), there is limited research on the beneficial effects of Se-Met in mitigating thermal stress and resisting nitrite stress in fish.
Spotted seabass (Lateolabrax maculatus) has become a major fish cultured in southern China due to its high nutritional and economic value (Cai et al., 2020). Its total production reached approximately 218,000 metric tons in 2022 (MARA, 2023). The optimal water temperature range for L. maculatus is from 16 to 28℃ (Wen et al., 2019). In summer, the water temperature in the main farming areas for L. maculatus often reaches 33℃ or higher along the southeast coast of China, leading to thermal stress that affects the growth, feed efficiency and immunity of L. maculatus (Li et al., 2023; Yuan et al., 2023). Providing an appropriate amount of Se via dietary Se-Met to L. maculatus is one such strategy to counter the oxidative stress caused by elevated water temperature. A complete literature search revealed that the dietary Se requirement of L. maculatus is yet to be reported. Thus, this study aimed to evaluate the interactive effects of different water temperatures (27 and 33℃) and dietary Se-Met levels on the growth, Se accumulation, antioxidant capacity, transcripts of selenoproteins and histological changes of muscle as well as resistance to nitrite stress in L. maculatus. The results will help us to understand the effects of Se-Met supplementation in L. maculatus at different temperatures and provide baseline information for the optimisation of feed for L. maculatus culture during different seasons.
2.　Materials and methods
Less
2.1.　 Animal ethics statement
In this study, we followed the ARRIVE guidelines (Animal Research: Reporting of In Vivo Experiments) to ensure the transparency and quality of our animal experiments. All procedures in this study were conducted following the guidelines of the Ethics Committee of Care and Use for Laboratory Animals of Jimei University (JMU202303004).
2.2.　 Preparation of Se-Met enriched diets
In this study, the formulation and proximate composition of the Se-amended diet for juvenile L. maculatus are shown in Table 1. The measured total Se levels in the control diets were 1.40 mg/kg Se dry weight (DW). Seleno-L-methionine (purity > 98%, Adisseo Life Science Co., Ltd., Shanghai, China) of 0.9, 1.8, 3.5 and 7.0 mg/kg DW (the nominal levels) was supplemented in the control diet to achieve the designated levels of total Se of 1.80, 2.45, 3.39 and 4.94 mg/kg, respectively. Feed pellets of approximately 2.5 mm diameter were prepared according to our previous research with modifications (Yuan et al., 2023). The feed was dried at 50℃ for 10 h, then stored at −20℃ until use.
2.3.　 Experimental design and feeding trial
Two thousand juvenile L. maculatus were obtained from a commercial fish breeding farm (Zhaoan, Fujian). To acclimate to the experimental aquaculture conditions, 2000 fish were evenly distributed across two aquariums (each with a volume of 1000 L per tank) set at pre-determined temperatures of 27 and 33℃, respectively. They were fed the same control diets twice daily for 2 weeks to acclimate to the experimental environment. After acclimation, 450 fish (1.09 ± 0.02 g) adapted to a water temperature of 27℃, and they were randomly grouped into fifteen 150 L tanks (30 fish per tank) of recirculating aquaculture systems, with a pre-set temperature of 27℃ (optimal temperature). Another 450 fish of the same size acclimated to 33℃ were transferred to another circulating water system consisting of 15 tanks with a pre-set temperature of 33℃. Out of the 15 tanks, three tanks (replicates) were allocated to each dietary Se-Met treatment. During the feeding trial for 10 weeks, fish were fed the Se-enriched diet at approximately 3% of their body weight twice daily at 08:00 and 17:00. Uneaten feed and faeces were removed after 30 min of feeding. The dechlorinated tap water was renewed, and feed intake was recorded daily. The conditions of the culture were as follows: water temperature at 27.0 ± 0.5℃ and 33 ± 0.5℃, 12 h/12 h light/dark photoperiod, total ammonia–nitrogen < 0.3 mg/L, dissolved oxygen ≥ 6 mg/L, and pH 7.0 to 7.5.
2.4.　 Sample collection
After the end of the feeding experiment, the experimental fish were starved for 24 h to purge the gut content, followed by euthanasia with eugenol (1:10,000; Sigma–Aldrich, USA). All fish in each tank were counted and weighed individually to calculate survival rate (SR) and weight gain. Blood samples from 9 fish per tank (with three fish pooled as one sample, n = 3) were randomly collected from the caudal vein and stored at 4℃. Blood was centrifuged at 850 × g at 4℃ for 10 min to obtain the serum samples. For measuring the total Se body burden and whole-body composition, two fish per replicate (n = 6) were selected and stored at −20℃. The livers of 2 fish per tank (n = 6) were collected for the antioxidant capacity measurement. Dorsal muscles of 2 fish per tank were collected for measuring the total Se levels and transcripts of genes related to selenoproteins and antioxidants (n = 6). The dorsal muscle of 2 fish per tank was fixed in Bouin's solution for histological examination (n = 6). Finally, the individual body and dissected liver were weighed to calculate the morphological parameters, i.e., hepatosomatic index and condition factor (Yu et al., 2023).
2.5.　 Proximate composition of diets, whole fish, and muscle
The proximate compositions of diets, whole-body and muscle samples were measured according to standard procedure (AOAC, 1995). Crude protein content was measured according to method 981.10 using a 2300 Auto-analyzer Kjeldahl System (FOSS, Hillerød, Denmark). Crude lipid content was analysed using Soxhlet's extraction, following method 960.39. For the determination of moisture content, samples were dried to a constant weight at 105℃, method 950.46. Crude ash content was measured by combustion using a muffle furnace at 550℃ for 8 h, method 942.05.
2.6.　 Determination of total Se content
The total Se content of the diets, whole body, and dorsal muscle was determined according to our previous method with slight modifications (Li et al., 2021). Briefly, approximately 0.2 g oven-dried diet samples, whole fish and muscle (n = 6) were digested with 10 mL of HNO3 (analysis grade, 68%) and 2 mL of HCl (analysis grade, 37%) (Aladdin, Shanghai, China) using a microwave digestion system at 170℃ for 45 min (MARS 6, CEM Co., Ltd, USA). After digestion, total Se concentrations in the diets and fish tissues were measured on an atomic fluorescence spectrometer (AFS-8300, Titan Co., Ltd, Beijing, China). The instrumental detection limit was 0.1 to 0.2 μg/L. For quality assurance and quality control (QA/QC), the recovery for total Se in the standard reference material (GBW10024, National Research Center for Certified Reference Materials, Beijing, China) was 98% to 105% of the certified value. Other QA/QC included spiked samples and acid blanks. One blank was carried out after every 5 samples.
2.7.　 Histological analysis in dorsal muscle
Histological analysis of the dorsal muscle samples was performed following a previous method with minor modifications (Liu et al., 2021). In brief, paraformaldehyde-fixed muscles were cut into pieces of approximately 0.3 cm3, followed by dehydration in graded alcohols and clearance in xylene. Afterwards, the muscle samples were embedded in paraffin wax, sectioned at 6 μm thickness, and stained with hematoxylin and eosin. Six randomly chosen fields of the muscle from each treatment were observed under a microscope (ECLIPSE Ni-U, Nikon, Japan). The diameter and density of muscle fibre per 1-mm2 field of view were determined using Image J software connected to the microscope (n = 6).
2.8.　 Antioxidant capacity analysis of serum and liver
To assess the antioxidant capacity of experimental fish, activities of glutathione peroxidase (GPx) and glutathione reductase (GR), levels of glutathione (GSH), oxidized glutathione (GSSG) and malondialdehyde (MDA) in the serum and liver samples were determined following the protocols of commercial assay kits from Jiancheng Bioengineering Institute (Nanjing, China).
2.9.　 RNA extraction and quantitative real-time PCR (qRT-PCR) assay
The total RNA extraction, RNA quantity and quality, synthesis of cDNA and qRT-PCR procedures were conducted following a previously described method with modifications (Li et al., 2021). Total RNA from the liver and muscle tissues were isolated using Trizol reagent (Vazyme Biotech Co., Ltd., Nanjing, China). RNA was quantified on a NanoDrop 2000 spectrophotometer (Wilmington, USA). The quality of RNA was assessed by 1.5% agarose gel electrophoresis.
The expression levels of 6 genes related to selenoproteins in the muscle and 6 genes related to antioxidants in the liver were determined using qRT-PCR. The sequences of the primers are shown in Table 2. In brief, the RT-qPCR program was run at 95℃ for 30 s, followed by 40 cycles of 95℃ for 15 s and 60℃ for 30 s. After the PCR reaction, melting curve analysis was performed to confirm the specificity of the genes. The expression of genes was normalized to β-actin and 18S using the 2−ΔΔCt method (Schmittgen and Livak, 2008).
2.10.　 Acute nitrite stress test
Prior to the acute nitrite stress, the lethal concentration for 50% mortality in 24 h (LC50-24 h) of L. maculatus reared at 27 and 33℃ was determined to be 73 and 57 mg/L, respectively. Based on the results of the acute toxicity test, the nominal concentrations of nitrite (sodium nitrite, AR, Macklin Biochemical Technology Co., Ltd., China) were set at 29.2 mg/L (27℃) and 22.8 mg/L (33℃) under different water temperatures. At the end of the 10-week feeding trial of dietary Se-Met, 12 fish per tank were selected and exposed to a predefined nitrite solution (120 L/tank) for 24 h to perform a nitrite stress test. During the 24-h exposure period, surviving individuals were recorded from each tank. In order to determine the changes in antioxidant parameters before and after nitrite stress, serum samples of 2 fish per replicate (two fish were pooled as one sample, n = 3) were collected at 0 and 24 h, respectively, then stored at −80℃.
2.11.　 Statistical analyses
All data are presented as mean ± standard error unless otherwise stated. Kolmogorov–Smirnov and Levene's tests were conducted to check the assumptions of normality and homogeneity of variance, respectively. Two-way analyses of variance (ANOVA) were used to check the differences in dietary Se treatments, water temperatures or their interaction with the measured parameters, followed by Tukey's test for multiple comparisons. All statistical analyses were performed using SPSS 26.0 software, and P < 0.05 was regarded as a significant difference. A multiple linear regression analysis was employed to determine the relationship between the dietary Se-Met level at which the maximum weight gain was obtained under two water temperatures.
3.　Results
Less
3.1.　 Growth performance and feed utilization
The growth performance and feed utilization of L. maculatus were significantly affected by water temperature and dietary Se-Met (Table 3). However, the interaction between water temperature and dietary Se-Met did not show a significant effect. Overall, the final body weight (FBW) and weight gain of L. maculatus reared at 33℃ were significantly lower (P < 0.001) than those of fish reared at 27℃. The FBW and weight gain of fish increased (P < 0.001) with dietary Se-Met levels from 0.9 to 3.5 mg/kg but decreased at 7.0 mg/kg, with the largest values obtained at 3.5 mg/kg. In contrast, FCR showed an opposite trend to FBW and weight gain (P < 0.001). Meanwhile, the cubic regression model analysis based on weight gain suggested that the optimal dietary Se-Met supplementation of L. maculatus was 2.39 and 4.46 mg/kg diet at 27 and 33℃, respectively (Fig. 1). In addition, fish survival was not significantly different among all treatments.
The morphological parameters of L. maculatus were influenced by temperature, but not by Se-Met or the interaction term of Se-Met × temperature (Table 3). The hepatosomatic index of L. maculatus reared at 33℃ treatment was significantly lower than at 27℃ treatment (P = 0.003), while condition factor showed an opposite result (P = 0.018).
3.2.　 Proximate composition analysis of the whole fish and muscle tissue
Proximate composition analysis of the whole fish and muscle tissue are reported in Table 4. The crude ash content of the whole fish, and the intramuscular crude lipid, and crude ash of L. maculatus reared at 33℃ were significantly higher (P < 0.001) than those of fish reared at 27℃. In contrast, the opposite was observed in the moisture of muscle (P < 0.001). The crude lipid content in the whole fish (P = 0.005) and muscle (P = 0.024) as well as intramuscular crude ash content (P < 0.001) was affected by temperature × Se-Met. Meanwhile, crude protein content in the whole fish and muscle was increased (P < 0.001) from 0.9 to 3.5 mg Se-Met/kg but decreased at 7.0 mg Se-Met/kg, with the highest values observed at 1.8 mg Se-Met/kg treatment. The crude lipid content in the whole fish was increased at 0.9 mg Se-Met/kg but decreased with higher Se-Met levels (P = 0.046), whereas crude lipid content of muscle was increased with increasing Se-Met levels (P < 0.001). The crude ash content in the whole fish was decreased at 1.8 mg Se-Met/kg then increased with higher Se-Met levels (P < 0.001), whereas intramuscular crude ash content was increased with increasing Se-Met levels (P = 0.037).
Dietary Se-Met × water temperature interaction significantly influenced the total Se content of muscle but not that of the whole fish (Fig. 2). Meanwhile, the total Se content of whole fish and muscle showed a dose-dependent increase with dietary Se-Met (P < 0.001). However, water temperatures had no significant effects on the total Se content of whole fish (P = 0.493) and muscle (P = 0.063).
3.3.　 Histological alteration in the muscle
The histological analysis showed that the fish muscle from both control and 7.0 mg Se-Met/kg treatments exhibited a typical pathological feature of fiber disintegration (Fig. 3A and B). Meanwhile, the diameter and density of muscle fiber were significantly affected by Se-Met and temperature (Fig. 3C and D). Overall, the diameter of the muscle fiber of L. maculatus reared at 33℃ was significantly larger (P = 0.007) than that of fish reared at 27℃, whereas muscle fiber density was reduced (P = 0.004). The diameter of muscle fiber was decreased (P = 0.001) with Se-Met levels from 3.5 to 7.0 mg/kg. The muscle fiber density was elevated (P = 0.001) at 0.9 mg/kg Se-Met but decreased from 1.8 to 7.0 mg Se-Met/kg, with the maximum density observed at 0.9 mg/kg Se-Met.
3.4.　 Antioxidant capacity in the serum and liver
Antioxidant parameters in the serum and liver of L. maculatus were all significantly affected by Se-Met and temperature, respectively (Tables 5 and 6). Overall, malondialdehyde (MDA) levels in the serum and liver of L. maculatus reared at 33℃ were significantly higher (P < 0.001) than those of fish reared at 27℃. The activity of GPx in the serum and activity of GR in the liver from the 33℃ treatments were lower (P < 0.001) than those from the 27℃ treatments; however, GPx activity in the liver followed the opposite trend (P = 0.036). Meanwhile, the activities of GPx, GR, and the levels of GSH in the serum (P = 0.012; P = 0.012; P = 0.003) and liver (P < 0.001; P < 0.001; P < 0.001) were enhanced when fed low levels of Se-Met but decreased (P < 0.05) afterwards with increased dietary Se-Met levels. In contrast, the opposite trend was witnessed in MDA levels from the serum (P < 0.001) and liver (P < 0.001).
3.5.　 Transcripts of genes related to antioxidants in the liver
Dietary Se-Met × water temperature interaction significantly influenced the transcripts of keap1, ap-1, and hsp70 (P < 0.001) but not those of nrf2 (P = 0.701), ho-1 (P = 0.547), and NF-kβ (P = 0.105) (Fig. 4). The transcriptional expression of keap1(P < 0.001) and NF-kβ (P = 0.001) in the liver from the 33℃ treatments was down-regulated (P < 0.01) compared to the 27℃ treatments. In contrast, the opposite was shown for ap-1 (P < 0.001) and hsp70 (P < 0.001). The transcriptional expression of ho-1 (P = 0.003), ap-1 (P < 0.001), and hsp70 (P < 0.001) was up-regulated in the liver by Se-Met from the 3.5 and 7.0 mg/kg treatments. The transcriptional expression of keap1 (P < 0.001) was up-regulated in treatments with 1.8 to 7.0 mg Se-Met/kg. In contrast, the transcript of NF-kβ was down-regulated (P = 0.037) in the 7.0 mg Se-Met/kg treatment.
3.6.　 Transcriptional expressions of selenoprotein genes in the muscle
There was a significant interaction effect between dietary Se-Met and water temperature on the transcripts of selenoprotein-related genes: txnrd1 (P < 0.001), dio2 (P < 0.001), gpx4a (P = 0.034), selt (P < 0.001), sep15 (P = 0.012), and selp (P < 0.001) in the muscle (Fig. 5). Overall, the transcripts of txnrd1 (P < 0.001), dio2 (P < 0.001), gpx4a (P < 0.001), selt (P < 0.001), sep15 (P = 0.038), and selp (P < 0.001) were up-regulated in the muscle by dietary Se-Met supplementation ranging from 1.8 to 7.0 mg/kg. The transcripts of txnrd1, selt, and selp in the muscle from the 33℃ treatments were down-regulated (P < 0.001) compared to those from the 27℃ treatments, whereas an opposite trend (P < 0.001) was found for gpx4a. However, the transcripts of dio2 (P = 0.578) and sep15 (P = 0.761) in the muscle of L. maculatus were not affected by water temperature.
3.7.　 Changes in serum antioxidant capacity after acute nitrite stress
After nitrite exposure for 24 h, the survival rate of L. maculatus cultured at 27 and 33℃ was 92% and 86%, respectively. Serum MDA levels, GSH/GSSH ratio, and GPx activity of L. maculatus cultured at 27 and 33℃ were significantly affected by dietary Se-Met and dissolved nitrite, respectively (Fig. 6). Relative to the control exposed for 0 h, serum MDA levels (P = 0.005; P < 0.001) and activity of GPx (P < 0.001; P = 0.006) in L. maculatus reared at both 27 and 33℃ were elevated after 24 h of exposure (Fig. 6A–D). In contrast, serum GSH/GSSG ratio (P < 0.001; P = 0.036) decreased in the 24 h of exposure treatments for all fish (Fig. 6E and F). Meanwhile, serum GPx activity (P = 0.042; P = 0.012) from two temperatures were affected by the interaction between dietary Se-Met and dissolved nitrite. Furthermore, the alterations in antioxidant physiology due to nitrite stress were consistent with the changes induced by varying levels of Se-Met.
4.　Discussion
Less
Se-Met is the dominant organic Se form in organisms, including fish (Sele et al., 2018; Stewart et al., 2004). The dietary route is predominant for the accumulation of Se in fish (Lemly, 2002). It has been shown that the level of Se-Met in the whole fish and tissues is positively correlated with dietary intake (Liu et al., 2017; Rider et al., 2009; Wang et al., 2018). In this study, there was a linear increase in total Se contents in the whole fish and muscle with increasing Se levels in the diet, regardless of the two culture temperatures. Similarly, Atlantic salmon (Salmo salar) fed dietary Se-Met accumulated Se mainly in the form of Se-Met in the whole fish, liver, and muscles (Lorentzen et al., 1994). Other similar results regarding Se accumulation have been reported in the hybrid striped bass (Morone saxatilis) and rainbow trout (Oncorhynchus mykiss) fed a Se-Met enriched diet over 8 weeks (Cotter et al., 2008; Wang et al., 2018). The fact that Se-Met accumulates in fish muscle strongly indicates its indispensability for fish, probably more specifically associated with the synthesis of selenoproteins (see discussion below) (Li et al., 2021; Wang et al., 2018).
As an essential micronutrient, Se plays an important role in growth promotion in fish, but has a narrow demarcation between beneficial and toxic effects (Janz et al., 2010). It is important to determine the optimal level of dietary Se-Met for cultured fish. In this study, diets supplemented with 0.9 to 3.5 mg Se-Met/kg increased the growth performance of L. maculatus. Growth performance decreased at 7.0 mg Se-Met/kg, indicating that optimal dietary Se-Met could improve the growth and feed utilization of L. maculatus and that excess Se-Met led to deleterious effects on fish growth. It has been shown that organic Se supplementation of 0.4 mg Se/kg could improve the growth and feed efficiency of blunt snout bream (Megalobrama amblycephala), while 0.8 mg Se/kg causes negative effects (Liu et al., 2017). Other similar results have been obtained in grouper (Epinephelus malabaricus) (Lin, 2014), Atlantic salmon (Berntssen et al., 2018), and Nile tilapia (Oreochromis niloticus) (Chen et al., 2020).
In the present study, water temperature also affected growth and feed utilization of L. maculatus independent of Se-Met level, with the inhibition of growth and feed utilization under high temperature conditions. This is consistent with the results of our previous research on the effects of elevated temperature (33℃) for L. maculatus (Cai et al., 2020; Li et al., 2023; Yuan et al., 2023). Early studies have demonstrated that the sub-optimal and supra-optimal water temperatures have a negative impact on growth (Xie et al., 2011) and feed utilization in tilapia (Likongwe et al., 1996). On the one hand, high-temperature induced thermal stress probably inhibits digestive capacity in L. maculatus (Yuan et al., 2023). On the other hand, fish reared at higher water temperatures need to allocate more resources and energy to maintain their basic metabolic functions rather than allocating it towards growth (Xie et al., 2011; Zeng et al., 2021). Furthermore, in this study, the optimal supplementation of 4.46 mg/kg for dietary Se-Met of L. maculatus reared at 33℃ was higher than that of 2.39 mg/kg of fish reared at 27℃. This indirectly implies that elevated water temperature induces thermal stress in fish, which in turn triggers a mechanism of selenium depletion to restore and maintain cellular homeostasis. Therefore, the nutrient requirements of Se-Met to achieve a maximal increase in weight gain of L. maculatus increase in high-temperature environments.
Previous data have shown that optimal levels of dietary Se-Met can improve the protein deposition in whole fish and tissues (Wang et al., 2021b), while excess Se accumulation will lead to adverse effects in fish (Lemly, 2002; Li et al., 2021; Liu et al., 2021). In this study, the content of crude protein was increased in the whole fish by supplementation of Se-Met at 1.8 mg/kg and was also increased in the muscle by Se-Met at 0.9 to 3.5 mg/kg. These findings are consistent with the result that dietary Se-yeast (containing >80% of Se-Met) improves the protein content in the muscle of O. mykiss, implying that optimal Se-Met may promote protein deposition by stimulating postprandial protein synthesis (Wang et al., 2021b). It is believed that both Se forms (organic and inorganic) can serve as an active substrate for various selenoproteins in the cells, whereas only Se-Met can be incorporated into proteins via non-specific Se-sulfur substitution without restriction (Janz et al., 2010; Schrauzer, 2000). This could account for the consisted results observed between the highest protein deposition and maximum WG in L. maculatus with increasing dietary Se-Met. However, the content of crude protein was lower in L. maculatus fed the diet containing 7.0 mg Se-Met/kg for 10 weeks, indicating that excess Se accumulation is likely to induce protein degradation for additional energy expenditure to counteract the adverse effects of excess Se (De et al., 2014). In this study, the crude lipid content was decreased in whole fish but increased in the muscle of L. maculatus as the dietary Se-Met level increased. Similarly, decreased lipid content in whole fish was witnessed in white sturgeon (Acipenser transmontanus) (Tashjian et al., 2006) and juvenile green sturgeon (A. medirostris) fed a Se-Met enriched diet (De et al., 2014). It has been found that Se causes dysregulation of lipid metabolism in the intestine of yellow catfish Pelteobagrus fulvidraco (Zhang et al., 2021). However, lipid deposition in muscle induced by Se has not been reported in fish species; its specific causes remain to be explored. Furthermore, in the present study, the muscular proximate composition of L. maculatus was altered by elevated water temperature, suggesting that the redistribution of energy in fish was possibly further triggered by thermal stress under elevated water temperature (Zhao et al., 2022). The effects of Se-Met on the proximate composition of muscle remain inconclusive, and further research is warranted.
Myofiber properties are crucial in determining muscle quality (Listrat et al., 2016). It has been reported that the proximate composition (i.e., moisture, lipid and collagen protein) of muscle is positively correlated with myofiber morphology (Dunajski, 1980; Periago et al., 2005). In this study, dietary Se-Met supplementation of 0.9 mg Se-Met/kg increased the density of muscular fibers. However, deficient or excess Se-Met decreased the diameter and density of muscular fibers, leading to further muscle fiber disintegration. Muscle degradation was also visually evident in the muscular histology from the control and 7.0 mg Se-Met/kg diets. Similarly, the optimal level of Se-Met added to feed may stimulate intermuscular binding ability and maintain the integrity of muscle fibers in fish (Liu et al., 2017). Meanwhile, compared to the fish from the 27℃ treatment, fish from the 33℃ treatment exhibited muscle fibers with a larger diameter, lower density, and more noticeable disintegration. Extremely high or low rearing water temperatures alter arrangement and density of muscle fibers in zebrafish (Johnston et al., 2009), which could prove that extreme temperature-stress alters the structure of muscle fibers in L. maculatus. Overall, thermal stress negatively impacts the muscle fibers of L. maculatus. However, the accumulation of appropriate Se-Met may help mitigate muscle disintegration caused by thermal stress, which may be attributed to the neutralization of excessive ROS by Se (Banh et al., 2016; Nakano et al., 2014). It is worth noting that excessive Se-Met may have the opposite effect.
In the intensive aquaculture industry, fish are often subjected to oxidative stress caused by various environmental factors (e.g., temperature) (Kim et al., 2016; Matthews and Berg, 1997). In general, oxidative stress occurs when there is an imbalance between the formation and removal of ROS in organisms (Torun et al., 2009). The accumulation of un-detoxified ROS can cause lipid peroxidative damage in the cell membrane (Su et al., 2019). Se is well known for its role in neutralizing ROS and maintaining redox balance in organisms (Weekley and Harris, 2013). In the present study, the MDA level in the serum and liver of L. maculatus decreased with dietary Se up to 1.8 mg Se-Met/kg and increased with higher dietary Se-Met level and thermal stress. Similarly, there was a negative correlation between the alteration of antioxidant-related indicators (i.e., GPx, GSH, and GR) and MDA levels of L. maculatus fed with Se-Met enriched diets. This result, together with those of previous studies (Ashouri et al., 2015; Ghaniem et al., 2022; Wang et al., 2018), confirms that optimal dietary Se-Met helps to prevent lipid peroxidation and maintain normal oxidative/antioxidant physiological homeostasis in fish via the rapid clearance of excessive ROS (Zhu et al., 2012). However, as our results have shown, elevated levels of Se-Met produce ROS beyond the scavenging capacity of antioxidants present in the organism, which can subsequently cause severe oxidative damage and possibly secondary decreased growth (Li et al., 2021; Liu et al., 2021; Palace et al., 2004; Tashjian et al., 2006). In addition, adaptive changes in GPx activity were observed in the serum and liver of L. maculatus reared at 33℃ under thermal stress, which further confirms the necessity of optimal dietary supplementation of Se-Met for maintaining normal antioxidant capacity in L. maculatus cultured at high temperatures.
Nuclear factor erythroid-2 related factor (nrf2) is a crucial regulator of the antioxidant response in organisms, and Kelch-like ECH-associated protein 1 (keap1) has been proven to interact with nrf2 (Ma, 2013; Wang et al., 2008). Nuclear factor -κβ (NF-κβ) and heme oxygenase (ho-1) can be induced in response to cellular stress caused by ROS (Ferrándiz and Devesa, 2008). It has been shown that cell antioxidation is related to the upregulation of ho-1, NF-κβ and ap-1 (Li et al., 2021; Zhao et al., 2021). In the present study, transcripts of ho-1, keap1, NF-κβ and ap-1 in the liver were increased with dietary Se-Met (except for a decreased transcript of NF-κβ in the liver of fish fed with 7 mg Se-Met/kg diet). These findings could imply that different Se-Met levels induce the up-regulation of Nrf2/NF-κβ, leading to the transcriptional activation of downstream antioxidant genes, including ho-1 and ap-1 (Zhao et al., 2021). HSP70 is a commonly used biomarker for stress in fish, which can inhibit intracellular protein denaturation and misfolding in fish exposed to stressful conditions (Iwama et al., 1999). In this study, the transcripts of hsp70 in the liver were up-regulated by dietary Se-Met supplementation of 3.5 to 7.0 mg Se-Met/kg under the thermal stress conditions. This is consistent with previous research that dietary nano-Se supplementation of 5 mg Se/kg induces the transcripts of hsp70 and hsp90 in the liver of O. mykiss under thermal stress (Li et al., 2022).
Selenoproteins perform a pleiotropic role in regulating physiological processes in fish (Tsuji et al., 2015). The beneficial effects of Se against oxidation are often attributed to the removal of various ROS by multiple families of selenoproteins (e.g., TXNRD, GPx, SEP15 and SelP) (Björnstedt et al., 1995; Weekley and Harris, 2013). GPx can catalyse the reduction of ROS to water or alcohol at the expense of consuming GSH (Weekley and Harris, 2013). In contrast, TXNRD plays a role in maintaining the intracellular redox status by utilizing NADPH to reduce thioredoxin (Arnér and Holmgren, 2000). SEP15 is a thiol-oxidoreductase-like selenoprotein involved in forming disulfide bonds to neutralize ROS (Tsuji et al., 2015). In the present study, transcriptional expression of txnrd, gpx4a, and selp in the muscle was enhanced with increased dietary Se-Met levels and an increased expression of sep15 by 7.00 mg Se-Met/kg diet at 27℃. DIO plays a crucial role in regulating thyroid hormones, growth, development, and immunity in fish (Saffari et al., 2018). In agreement with these findings, up-regulated transcripts of gpx4b, txnrd, selp have been observed in the muscle and liver of O. mykiss fed an optimal level of dietary Se-Met at 2 to 6 mg Se/kg diet (Wang et al., 2018). The present study also evidenced that optimal Se-Met up-regulated the transcripts of dio2 in the muscle of L. maculatus. These results suggest that an optimal level of Se-Met in fish feed could promote Se accumulation in the muscle, which could stimulate the expression of antioxidant-related selenoproteins. Meanwhile, DIO may resist thermal stress by regulating the synthesis and metabolism of thyroid hormone, whereas disruption of dio2 leads to a state of localized hypothyroidism (Drigo et al., 2013). In the present study, when fish were fed Se-Met enriched diets of 3.5 to 7.0 mg/kg, the transcripts of dio2 in fish reared at 33℃ were significantly lower than those reared at 27℃. This implies that thermal stress affects the production and metabolism of thyroxine in fish and interferes with the production of triiodothyronine (T3), which may also be one of the reasons for the decline in fish growth under thermal stress.
Furthermore, thermal stress inhibited the transcripts of these selenoproteins in muscle, which is consistent with the fact that high temperatures result in the disruption of enzymes and denaturation of proteins in fish (Dalvi et al., 2009). Previous research also suggests that the transcripts of gpx1a and txnrd in the liver of O. mykiss are induced by acute thermal stress but are inhibited by chronic heat stress (Li et al., 2022). These findings may indicate that increased expression levels of gpx1a and txnrd are helpful in reducing oxidative damage in organisms. However, the activity of these selenoproteins is insufficient to effectively counteract chronic oxidative stress, leading to concurrent transcriptional inhibition of selenoproteins (Li et al., 2022).
Nitrite () is produced as an intermediate product during bacterial nitrification and denitrification processes (Jensen, 2003). It can be accumulated in intensive aquaculture systems. Once accumulated in excess, it has toxic effects on aquatic organisms (Wang et al., 2019). In the present study, compared with the control fish, increased MDA levels and GPx activity, as well as decreased GSH/GSSG, were observed in fish cultured at different temperatures after 24 h of nitrite exposure. Meanwhile, relative to fish reared at 27℃, nitrite exposure in fish cultured at 33℃ exacerbated oxidative stress even further, resulting in higher MDA levels in various Se-Met feeding treatments. These findings suggest that exposure to nitrite leads to an increase in ROS levels in organisms, which is further amplified by thermal stress. However, the antioxidant defense system activated by optimal dietary Se-Met can partially mitigate the oxidative stress induced by those two environmental factors (Li et al., 2022), as evidenced by the increase in GPX activity and the GSH/GSSG ratio observed in the 0.9 to 1.8 mg/kg Se-Met treatments. Similar studies have reported that different aquatic animal species fed with organic Se-enriched diets decreased levels of MDA in tissues and effectively enhanced resistance to nitrite stress (Long et al., 2017; Wang et al., 2019; Wang et al., 2020).
5.　Conclusion
Less
In summary, this study demonstrates that thermal stress induced by elevated water temperature (33℃) results in reduced growth and antioxidant capacity of tissues, alters the proximate composition and histological structure of muscle, inhibits the transcripts of muscle selenoproteins, and exacerbates oxidative damage caused by nitrite stress in L. maculatus. However, dietary supplementation of Se-Met enhances the growth, antioxidant capacity, transcripts of selenoproteins, improves the histology structure of muscle, and enhances the resistance to nitrite stress of L. maculatus fed on Se-Met enriched diets at a maximum of 3.5 mg Set-Met/kg for 10-weeks. Based on cubic regression analyses of weight gain, the optimal dietary supplementation of Se-Met for L. maculatus to achieve maximal growth is 2.39 and 4.46 mg Se-Met/kg reared at 27 and 33℃, respectively. Meanwhile, based on the results of serum antioxidant capacity after nitrite stress, it can be concluded that dietary Se-Met supplementation of 0.9 to 1.8 mg Se-Met/kg can achieve the optimal antioxidant capacity of L. maculatus at both temperatures. Overall, considering the effects of dietary Se-Met on the growth, antioxidant capacity and resistance to nitrite stress of L. maculatus, this study suggests that the range of Se-Met supplementation in diets of L. maculatus is 1.80 to 2.39 mg Se-Met/kg of the diet at 27℃ and 1.80 to 4.46 mg Se-Met/kg of the diet at 33℃.
References
Less
AOAC. Official methods of analysis. 16th ed. Arlington, VA, USA: Association of Official Analytical Chemists; 1995.
Arnér ESJ, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 2000;267:6102-9.
Ashouri S, Keyvanshokooh S, Salati AP, Johari SA, Pasha-Zanoosi H. Effects of different levels of dietary selenium nanoparticles on growth performance, muscle composition, blood biochemical profiles and antioxidant status of common carp (Cyprinus Carpio). Aquaculture 2015;446:25-9.
Banh S, Wiens L, Sotiri E, Treberg JR. Mitochondrial reactive oxygen species production by fish muscle mitochondria: potential role in acute heat-induced oxidative stress. Comp Biochem Physiol B Biochem Mol Biol 2016;191:99-107.
Bansemer MS, Stone DAJ, D'Antignana T, Skordas P, Kuerschner L, Currie KL. Optimizing feeding strategies for yellowtail jack at winter water temperatures. N Am J Aquacult 2018;80:128-40.
Berntssen MH, Betancor M, Caballero MJ, Hillestad M, Rasinger J, Hamre K, et al. Safe limits of selenomethionine and selenite supplementation to plant-based Atlantic salmon feeds. Aquaculture 2018;495:617-30.
Björnstedt M, Hamberg M, Kumar S, Xue J, Holmgren A. Human thioredoxin reductase directly reduces lipid hydroperoxides by NADPH and selenocystine strongly stimulates the reaction via catalytically generated selenols. J Biol Chem 1995;270:11761-4.
Buentello JA, Gatlin IIIDM, Neill WH. Effects of water temperature and dissolved oxygen on daily feed consumption, feed utilization and growth of channel catfish (Ictalurus punctatus). Aquaculture 2000;182:339-52.
Cai LS, Wang L, Song K, Lu KL, Zhang CX, Rahimnejad S. Evaluation of protein requirement of spotted seabass (Lateolabrax maculatus) under two temperatures, and the liver transcriptome response to thermal stress. Aquaculture 2020;516:734615.
Chen H, Li J, Yan L, Cao J, Li D, Huang GY, et al. Subchronic effects of dietary selenium yeast and selenite on growth performance and the immune and antioxidant systems in Nile tilapia Oreochromis niloticus. Fish Shellfish Immunol 2020;97: 283-93.
Cheng CH, Guo ZX, Luo SW, Wang AL. Effects of high temperature on biochemical parameters, oxidative stress, DNA damage and apoptosis of pufferfish (Takifugu obscurus). Ecotoxicol Environ Saf 2018;150:190-8.
Cotter PA, Craig SR, McLean E. Hyperaccumulation of selenium in hybrid striped bass: a functional food for aquaculture? Aquacult Nutr 2008;14:215-22.
Dalvi RS, Pal AK, Tiwari LR, Das T, Baruah K. Thermal tolerance and oxygen consumption rates of the catfish Horabagrus brachysoma (Günther) acclimated to different temperatures. Aquaculture 2009;295:116-9.
De Riu N, Lee JW, Huang SS, Moniello G, Hung SS. Effect of dietary selenomethionine on growth performance, tissue burden, and histopathology in green and white sturgeon. Aquat Toxicol 2014;148:65-73.
Drigo RA, Fonseca TL, Werneck-de-Castro JPS, Bianco AC. Role of the type 2 iodothyronine deiodinase (D2) in the control of thyroid hormone signaling. Biochim Biophys Acta Gen Subj 2013;1830:3956-64.
Dunajski E. Texture of fish muscle. J Texture Stud 1980;10:301-18.
Ferrándiz ML, Devesa I. Inducers of heme oxygenase-1. Curr Pharmaceut Des 2008;14:473-86.
Gatlin IIIDM, Wilson RP. Dietary selenium requirement of fingerling channel catfish. J Nutr 1984;114:627-33.
Ghaniem S, Nassef E, Zaineldin AI, Bakr A, Hegazi S. A comparison of the beneficial effects of inorganic, organic, and elemental nano-selenium on Nile tilapia: growth, immunity, oxidative status, gut morphology, and immune gene expression. Biol Trace Elem Res 2022;200:5226-41.
Iwama GK, Vijayan MM, Forsyth RB, Ackerman PA. Heat shock proteins and physiological stress in fish. Am Zool 1999;39:901-9.
Janz DM, DeForest DK, Brooks ML, Chapman PM, Gilron G, Hoff D, et al. Selenium toxicity to aquatic organisms. In: Chapman PM, Adams WJ, Brooks ML, Delos CG, Luoma SN, Maher WA, Ohlendorf HM, Presser TS, Shaw DP, editors. Ecological assessment of selenium in the aquatic environment. Boca Raton, FL: CRC Press; 2010. p. 141-231.
Jensen FB. Nitrite disrupts multiple physiological functions in aquatic animals. Comp Biochem Physiol Part A Mol Integr 2003;135:9-24.
Johnston IA, Lee HT, Macqueen DJ, Paranthaman K, Kawashima C, Anwar A, et al. Embryonic temperature affects muscle fibre recruitment in adult zebrafish: genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes. J Exp Biol 2009;212:1781-93.
Kim BS, Jung SJ, Choi YJ, Kim NN, Choi CY, Kim JW. Effects of different light wavelengths from LEDs on oxidative stress and apoptosis in olive flounder (Paralichthys olivaceus) at high water temperatures. Fish Shellfish Immunol 2016;55: 460-8.
Kim JH, Park HJ, Kim KW, Hwang IK, Kim DH, Oh CW, et al. Growth performance, oxidative stress, and non-specific immune responses in juvenile sablefish, Anoplopoma fimbria, by changes of water temperature and salinity. Fish Physiol Biochem 2017;43:1421-31.
Lemly AD. Symptoms and implications of selenium toxicity in fish: the Belews Lake case example. Aquat Toxicol 2002;57:39-49.
Li L, Liu Z, Quan J, Lu J, Zhao G, Sun J. Dietary nanoselenium supplementation for heat-stressed rainbow trout: effects on organizational structure, lipid changes, and biochemical parameters as well as heat-shock-protein-and selenoproteinrelated gene expression. Fish Physiol Biochem 2022;48:707-22.
Li X, Liu H, Li D, Lei H, Wei X, Schlenk D, et al. Dietary seleno-L-methionine causes alterations in neurotransmitters, ultrastructure of the brain, and behaviors in zebrafish (Danio rerio). Environ Sci Technol 2021;55:11894-905.
Li X, Sun J, Wang L, Song K, Lu K, Zhang L, et al. Effects of dietary vitamin E levels on growth, antioxidant capacity and immune response of spotted seabass (Lateolabrax maculatus) reared at different water temperatures. Aquaculture 2023;565:739141.
Likongwe JS, Stecko TD, Stauffer JR, Carline RF. Combined effects of water temperature and salinity on growth and feed utilization of juvenile Nile tilapia Oreochromis niloticus (Linneaus). Aquaculture 1996;146:37-46.
Lin YH. Effects of dietary organic and inorganic selenium on the growth, selenium concentration and meat quality of juvenile grouper Epinephelus Malabaricus. Aquaculture 2014;430:114-9.
Listrat A, Lebret B, Louveau I, Astruc T, Bonnet M, Lefaucheur L, et al. How muscle structure and composition influence meat and flesh quality. Sci World J 2016;2016:3182746.
Liu GX, Jiang GZ, Lu KL, Li XF, Zhou M, Zhang DD, et al. Effects of dietary selenium on the growth, selenium status, antioxidant activities, muscle composition and meat quality of blunt snout bream, Megalobrama amblycephala. Aquacult Nutr 2017;23:777-87.
Liu H, Li X, Lei H, Li D, Chen H, Schlenk D, et al. Dietary seleno-L-methionine alters the microbial communities and causes damage in the gastrointestinal tract of Japanese medaka Oryzias latipes. Environ Sci Technol 2021;55:16515-25.
Long M, Lin W, Hou J, Guo H, Li L, Li D, et al. Dietary supplementation with selenium yeast and tea polyphenols improve growth performance and nitrite tolerance of Wuchang bream (Megalobrama amblycephala). Fish Shellfish Immunol 2017;68: 74-83.
Lorentzen M, Maage A, Julshamn K. Effects of dietary selenite or selenomethionine on tissue selenium levels of Atlantic salmon (Salmo salar). Aquaculture 1994;121:359-67.
Ma Q. Role of Nrf2 in oxidative stress and toxicity. Annu Rev Pharmacol Toxicol 2013;53:401-26.
MARA (Ministry of Agriculture and Rural Affairs of the People's Republic of China). China fishery statistical yearbook. Beijing, China: China Agriculture Press; 2023.
Mariotti M, Ridge PG, Zhang Y, Lobanov AV, Pringle TH, Guigo R, et al. Composition and evolution of the vertebrate and mammalian selenoproteomes. PLoS One 2012;7:e33066.
Matthews KR, Berg NH. Rainbow trout responses to water temperature and dissolved oxygen stress in two southern California stream pools. J Fish Biol 1997;50:50-67.
Mechlaoui M, Dominguez D, Robaina L, Geraert PA, Kaushik S, Saleh R, et al. Effects of different dietary selenium sources on growth performance, liver and muscle composition, antioxidant status, stress response and expression of related genes in gilthead seabream (Sparus aurata). Aquaculture 2019;507:251-9.
Nakano T, Kameda M, Shoji Y, Hayashi S, Yamaguchi T, Sato M. Effect of severe environmental thermal stress on redox state in salmon. Redox Biol 2014;2: 772-6.
Palace VP, Spallholz JE, Holm J, Wautier K, Evans RE, Baron CL. Metabolism of selenomethionine by rainbow trout (Oncorhynchus mykiss) embryos can generate oxidative stress. Ecotoxicol Environ Saf 2004;58:17-21.
Periago MJ, Ayala MD, López-Albors O, Abdel I, Martínez C, García-Alcázar A. Muscle cellularity and flesh quality of wild and farmed sea bass, Dicentrarchus labrax L. Aquaculture 2005;249:175-88.
Rider SA, Davies SJ, Jha AN, Fisher AA, Knight J, Sweetman JW. Supra-nutritional dietary intake of selenite and selenium yeast in normal and stressed rainbow trout (Oncorhynchus mykiss): implications on selenium status and health responses. Aquaculture 2009;295:282-91.
Saffari S, Keyvanshokooh S, Zakeri M, Johari SA, Pasha-Zanoosi H, Mozanzadeh MT. Effects of dietary organic, inorganic, and nanoparticulate selenium sources on growth, hemato-immunological, and serum biochemical parameters of common carp (Cyprinus carpio). Fish Physiol Biochem 2018;44:1087-97.
Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc 2008;3:1101-8.
Schrauzer GN. Selenomethionine: a review of its nutritional significance, metabolism and toxicity. J Nutr 2000;130:1653-6.
Sele V, Ørnsrud R, Sloth JJ, Berntssen MH, Amlund H. Selenium and selenium species in feeds and muscle tissue of Atlantic salmon. J Trace Elem Med Biol 2018;47:124-33.
Stewart AR, Luoma SN, Schlekat CE, Doblin MA, Hieb KA. Food web pathway determines how selenium affects aquatic ecosystems: A San Francisco Bay case study. Environ Sci Technol 2004;38:4519-26.
Su LJ, Zhang JH, Gomez H, Murugan R, Hong X, Xu D, et al. Reactive oxygen speciesinduced lipid peroxidation in apoptosis, autophagy, and ferroptosis. Oxid Med Cell Longev 2019;2019:5080843.
Tashjian DH, Teh SJ, Sogomonyan A, Hung SSO. Bioaccumulation and chronic toxicity of dietary L-selenomethionine in juvenile white sturgeon (Acipenser transmontanus). Aquat Toxicol 2006;79:401-9.
Torun AN, Kulaksizoglu S, Kulaksizoglu M, Pamuk BO, Isbilen E, Tutuncu NB. Serum total antioxidant status and lipid peroxidation marker malondialdehyde levels in overt and subclinical hypothyroidism. Clin Endocrinol 2009;70:469-74.
Tsuji PA, Carlson BA, Yoo MH, Naranjo-Suarez S, Xu XM, He Y, et al. The 15kDa selenoprotein and thioredoxin reductase 1 promote colon cancer by different pathways. PLoS One 2015;10:e0124487.
Vinagre C, Madeira D, Narciso L, Cabral HN, Diniz M. Effect of temperature on oxidative stress in fish: lipid peroxidation and catalase activity in the muscle of juvenile seabass, Dicentrarchus labrax. Ecol Indicat 2012;23:274-9.
Wang C, Lovell RT. Organic selenium sources, selenomethionine and selenoyeast, have higher bioavailability than an inorganic selenium source, sodium selenite, in diets for channel catfish (Ictalurus punctatus). Aquaculture 1997;152:223-34.
Wang L, Li X, Lu K, Song K, Wang G, Zhang C. Dietary hydroxyl methionine selenium supplementation enhances growth performance, antioxidant ability and nitrite tolerance of Litopenaeus vannamei. Aquaculture 2021a;537:736513.
Wang L, Wang L, Zhang D, Li S, Yin J, Xu Z, et al. Effect of dietary selenium on postprandial protein deposition in the muscle of juvenile rainbow trout (Oncorhynchus mykiss). Br J Nutr 2021b;125:721-31.
Wang L, Zhang X, Wu L, Liu Q, Zhang D, Yin J. Expression of selenoprotein genes in muscle is crucial for the growth of rainbow trout (Oncorhynchus mykiss) fed diets supplemented with selenium yeast. Aquaculture 2018;492:82-90.
Wang X, Shen Z, Wang C, Li E, Qin JG, Chen L. Dietary supplementation of selenium yeast enhances the antioxidant capacity and immune response of juvenile Eriocheir Sinensis under nitrite stress. Fish Shellfish Immunol 2019;87:22-31.
Wang XJ, Sun Z, Chen W, Li Y, Villeneuve NF, Zhang DD. Activation of Nrf2 by arsenite and monomethylarsonous acid is independent of Keap1-C151: enhanced Keap1-Cul3 interaction. Toxicol Appl Pharmacol 2008;230:383-9.
Wang Y, Han J, Li W, Xu Z. Effect of different selenium source on growth performances, glutathione peroxidase activities, muscle composition and selenium concentration of allogynogenetic crucian carp (Carassius auratus gibelio). Anim Feed Sci Technol 2007;134:243-51.
Weekley CM, Harris HH. Which form is that? The importance of selenium speciation and metabolism in the prevention and treatment of disease. Chem Soc Rev 2013;42:8870-94.
Wen HS, Li JF, Zhang MZ, Li Y, Qi X, Zhang KQ, et al. Physiology and breeding technology of seabass in mariculture. Beijing: China Agricultural Press; 2019. p. 183-6.
Xie S, Zheng K, Chen J, Zhang Z, Zhu X, Yang Y. Effect of water temperature on energy budget of Nile tilapia (Oreochromis niloticus). Aquacult Nutr 2011;3: 683-90.
Yu MH, Li XS, Wang J, Longshaw M, Song K, Wang L, et al. Substituting fish meal with a bacteria protein (Methylococcus capsulatus, Bath) grown on natural gas: effects on growth non-specific immunity and gut health of spotted seabass (Lateolabrax maculatus). Anim Feed Sci Technol 2023;296:115556.
Yuan J, Li X, Song K, Li X, Zhang C, Lu K, et al. Effects of dietary zinc levels on growth, intestinal health, antioxidant and non-specific immunity of spotted seabass (Lateolabrax maculatus) reared at two temperatures. Aquaculture 2023;577: 739959.
Zak MA, Manzon RG. Expression and activity of lipid and oxidative metabolism enzymes following elevated temperature exposure and thyroid hormone manipulation in juvenile lake whitefish (Coregonus clupeaformis). Gen Comp Endocrinol 2019;275:51-64.
Zeng NN, Jiang M, Wen H, Liu W, Wu F, Tian J, et al. Effects of water temperatures and dietary protein levels on growth, body composition and blood biochemistry of juvenile GIFT tilapia (Oreochromis niloticus). Aquacult Nutr 2021;27:240-51.
Zhang DG, Zhao T, Xu XJ, Lv WH, Luo Z. Dietary marginal and excess selenium increased triglycerides deposition, induced endoplasmic reticulum stress and differentially influenced selenoproteins expression in the anterior and middle intestines of yellow catfish Pelteobagrus fulvidraco. Antioxidants 2021;10:535.
Zhao H, Ke H, Zhang L, Zhao Z, Lai J, Zhou J, et al. Integrated analysis about the effects of heat stress on physiological responses and energy metabolism in Gymnocypris chilianensis. Sci Total Environ 2022;806:151252.
Zhao H, Wang Y, Liu Y, Yin K, Wang D, Li B, et al. ROS-induced hepatotoxicity under cypermethrin: involvement of the crosstalk between Nrf2/Keap1 and NF-κB/iκB-α pathways regulated by proteasome. Environ Sci Technol 2021;55: 6171-83.
Zhu Y, Chen Y, Liu Y, Yang H, Liang G, Tian L. Effect of dietary selenium level on growth performance, body composition and hepatic glutathione peroxidase activities of largemouth bass Micropterus salmoide. Aquacult Res 2012;43: 1660-8.
Appendix
Less
Year 2024 volume 19 Issue 1
PDF
92
49
Cite this Article
BibTeX
Article Info
doi: 10.1016/j.aninu.2023.12.013
  • Receive Date：2023-08-30
  • Online Date：2026-01-28
  • Published：2024-12-10
Article Data
Affiliations
History
  • Received：2023-08-30
  • Revised：2023-12-14
  • Accepted：2023-12-19
Affiliations
    Xiamen Key Laboratory for Feed Quality Testing and Safety Evaluation, Fisheries College, Jimei University, Xiamen 361021, China

Corresponding:

*

Corresponding author. E-mail address: (L. Wang).
References
Share
https://castjournals.cast.org.cn/joweb/aninu/EN/10.1016/j.aninu.2023.12.013
Share to
QR

Scan QR to access full text

Cite this article
BibTeX
Citations
表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
关闭全屏
  • BibTeX
  • EndNote
  • RefWorks
  • TxT
Links
Articles
Latest Articles
Most Read
Collections
Updates
Events
News
Multimedia
About
About Us
Contact
No. 86 Xueyuan South Road, Haidian District, Beijing
100081
010-62199257
qkjq@cast.org.cn

Copyright © 2025 China Association for Science and Technology. All rights reserved. For all open access content, the relevant licensing terms apply.
Sponsored by the Office of the Leading Group for Cybersecurity and Informatization of CAST, and supported by Science and Technology Review Publishing House