Zi-Meng Li
Xiu-Li Wang1,2
Jia-Qiang Huang- 1The Key Laboratory of Pufferfish Breeding and Culture in Liaoning Province, Dalian Ocean University, Dalian, China
- 2College of Fisheries an Life, Dalian Ocean University, Dalian, Liaoning, China
- 3Hebei Key Laboratory of Ocean Dynamics Resources and Environments, Hebei Normal University of Science and Technology, Qinhuangdao, China
- 4Department of Nutrition and Health, China Agricultural University, Beijing, China
There will be generated some adverse conditions in the process of acquculture farming with the continuous improvement of the intensive degree of modern aquaculture, such as crowding stress, hypoxia, and malnutrition, which will easily lead to oxidative stress. Se is an effective antioxidant, participating and playing an important role in the antioxidant defense system of fish. This paper reviews the physiological functions of selenoproteins in resisting oxidative stress in aquatic animals, the mechanisms of different forms of Se in anti-oxidative stress in aquatic animals and the harmful effects of lower and higher levels of Se in aquaculture. To summarize the application and research progress of Se in oxidative stress in aquatic animals and provide scientific references for its application in anti-oxidative stress in aquaculture.
1 Introduction
Selenium (Se) is an essential micronutrient that maintains growth, health and development in human and animals (Hatfield et al., 2012). Se exists in nature is available as inorganic form and organic form. In addition, there is also a new type of synthetic nano form. The biological functions of Se include promoting the growth and development of animals, improving the antioxidant capacity of the body, avoiding oxidative stress, enhancing immunity, improving the health of the body, and are widely used in the growth and development of aquaculture animals (Wischhusen et al., 2020; Khan et al., 2017; Jingyuan et al., 2020). However, Se cannot be directly digested and absorbed by organisms. Se appears functions in the form of selenoprotein and exerts multiple and complex effects (Wrobel et al., 2016).
There will be generated some adverse conditions in the process of aquaculture farming with the continuous improvement of the intensive degree of modern aquaculture, such as crowding stress, hypoxia, and malnutrition. Meanwhile, that will promote the production of excessive reactive oxygen species (ROS), change the balance of oxidation and reduction in cells and will lead to oxidative stress (Rider et al., 2009; Abdel Tawwab et al., 2019). Once oxidative stress occurs, it may lead to the dynamic imbalance of free radical stability, which ultimately the fish poor growth and decline the meat quality (Chadio et al., 2015). The damage of oxidative stress in production is increasingly prominent, so it is urgent to solve the problem of oxidative stress in aquaculture animals.
In order to prevent oxidative damage caused by adverse conditions, aquaculture animals must have an effective antioxidant system, such as endogenous free radical scavenging enzymes and exogenous antioxidants (Ighodaro and Akinloye, 2018). Se is just a extra-effective antioxidant and plays an important role in the antioxidant defense mechanism of fish. It protects the cell membrane from oxidative damage through regulate glutathione peroxidase (GPX) activity (Hamilton, 2004). Se can decompose and clear peroxides, thus preventing the accumulation of reactive oxygen species and free radicals such as hydrogen peroxide (H2O2) in the body tissues (Zuo et al., 2019), enhancing resistance to inflammation, maintaining immune function and stabilizing the internal environment (Wande et al., 2020). However, dietary Se deficiency will reduce the expression of selenoproteins, increase the peroxidation reaction of lipids, proteins, DNA and then pose a threat to the health of the body (Rao et al., 2020). Excessive Se will also produce toxic side effects on the body, leading to liver damage, physiological function decline, immune capacity reduction, and even death (Chadio et al., 2015).
At present, the research on Se antioxidant stress has involved inorganic Se (such as sodium selenite), organic Se (such as yeast Se, selenomethionines) and nano Se. In the study of the effects of sodium selenite and lactobacillus on the growth and immune response of rainbow trout, the results showed that the use of sodium selenite and lactobacillus as feed additives could improve the growth and metabolism. Also, the effect of lactobacillus on the natural immune response of rainbow trout was also enhanced under the effect of selenite (Kousha et al., 2020). Another study found that, the mortality rate and malondialdehyde (MDA) level of grass carp fed a high-fat diet supplemented with 0.3 and 0.6 mg/kg nano Se was significantly reduced after hypoxia stress, indicating that nano Se can alleviate lipid peroxidation, thus alleviating the oxidative damage of grass carp under hypoxia stress (Yu et al., 2020). Liu et al. (2017) showed that 0.4 mg/kg yeast Se significantly increased the activity of catalase (CAT) and GPX in the liver of blunt snout bream and significantly decreased the activity of glutathione reductase (GR) and the content of MDA, showing strong antioxidant capacity.
2 The role of selenoproteins in the antioxidant system of aquatic animals
In general, Se sources in animals will first be converted into selenides for play on organisms and then will be converted into proteins containing selenocysteine (Sec), that is, selenoprotein which then will be absorbed and used by organisms (Yoboue et al., 2018). During the process of fish growth, any pressure condition will directly or indirectly cause oxidative stress, leading to the level of intracellular ROS related to oxidative stress increasing, causing destructive effects on lipids, proteins, and DNA (Martínez Álvarez et al., 2005; Zenteno Savín et al., 2006). The lack of balance between the production of ROS and the antioxidant defense system of animals will lead to DNA hydroxylation, protein denaturation, lipid peroxidation, cell apoptosis, ultimately lead to cell damage (Yang et al., 2016). As an effective antioxidant, Se plays an important role in the antioxidant defense system of aquaculture animals. It can maintain balance in the body and antioxidant system by generating and removing ROS (Steinbrenner and Sies, 2009).
It has been found that the thioredoxin reductase system and glutathione peroxidase system play an important role in cellular oxidative stress defense (Lee et al., 2012; Benfeitas et al., 2014). The main function of GPX in mammals is to eliminate excessive free radicals in cells, including superoxide anions (O2-), H2O2, and hydroxyl radicals (OH−). Then through reduce peroxides to corresponding alcohols, prevent lipid peroxidation, and regulate the balance of redox in cells (Yoboue et al., 2018; Rocca et al., 2018). The Thioredoxin system is one of the main redox buffer systems in the body, which plays a key role in the transduction of redox signals (Canter et al., 2021; Shchedrina et al., 2010). In addition, the endoplasmic reticulum (ER) is one of the important places where redox reactions occur in cells, which can produce H2O2 and ROS (Varlamova, 2018). SELENOF, Recombinant Deiodinase, Iodothyronine, Type II (DIO2), SELENOS, SELENON, SELENOK, SELENOM, and SELENOT are considered to be seven endoplasmic reticulum resident proteins with oxidoreductase activity and can participate in a series of processes, such as the regulation of endoplasmic reticulum redox state, endoplasmic reticulum stress and intracellular Ca2+ homeostasis (Malandrakis et al., 2014; Pitts and Hoffmann, 2017; Drew et al., 2008; Addinsall et al., 2018; Rathore et al., 2021; Xu et al., 2022) Specific selenoprotein involved in redox reaction are shown in Table 1.
TABLE 1. Antioxidant functions of releated selenoproteins.
3 Application of different forms of Se on antioxidant system of aquatic animals
In many studies, Se has been found that supplement oxidative stress caused by hypoxia, crowding, heavy metal pollution, intake oxidized oil and other pressure conditions (Schieber and Chandel, 2014; Chen et al., 2013). Oxidative stress is considered to be a major problem in aquaculture because it is reported that this phenomenon will occur naturally in most aquatic environments, especially in high-density intensive fish farming which will induce metabolic changes and produce a large number of reactive oxygen species (Zenteno Savín et al., 2006). In order to avoid the imbalance of ROS production, aquatic animals can reduce the formation of ROS or reduce the high reactivity of such compounds through antioxidant components which are produced by cells (endogenous sources) or obtained through diet (exogenous sources). A Lack of balance between ROS formation and the ability of organisms to process reactive oxygen will lead to oxidative stress (Wang et al., 2013; Ji et al., 2019). At present, many aquatic animals have been studied on the antioxidant system, and there is evidence that they can prevent or repair oxidative damage (Biller and Takahashi, 2018) (Table 2).
TABLE 2. Effects of different forms of Se on the antioxidant system of aquatic animals.
4 Harmful effects of Se deficiency and excess on antioxidant function in aquatic animals
After these environmental pressures, Se may have protective effects on the pathology related to oxidative stress of aquatic animals. It is particularly important for intensive aquaculture animals, because environmental pressures may cause significant losses to fish growers. The demand for Se will increase after suffering environmental pressures, and supplementation is a necessary condition to meet the needs of fish growth (Ashouri et al., 2015). Se can act as a dietary supplement to effectively improve the oxidation status of aquaculture animals. Although, dietary Se application in aquatic animal feed is considered to have a narrow intake range for high concentration may be toxic (Nasir et al., 2015) and lack may have adverse effects on fish health, leading to tissue damage and physiological function weakening (Khan and Bano, 2016). Therefore, their safety in aquaculture animals is controversial.
4.1 Harmful effects of selenium excess
Se is an essential micronutrient required for fish, which plays an important role in the antioxidant system and also affects the lipid metabolism, sugar metabolism and amino acid metabolism of aquatic animals (Yoboue et al., 2018; Fontagné Dicharry et al., 2015; Abdel Tawwab et al., 2007). Although Se supplementation in aquatic feed can alleviate the oxidation state of cultured animals, but excessive Se content will also have some toxic effects (Jobling, 2012). When the Se content in the aquatic feed is slightly higher than the demand, it will have other adverse effects including oxidative stress, cytotoxicity and genotoxicity (Gobi et al., 2018). If the fish is exposed to excessive Se, the degree of oxidative stress in the body can be significantly increased, then cause oxidative stress. Glutathione (GSH) is largely used to maintain the homeostasis of ROS in the body, can cause an imbalance in the antioxidant system (Atencio et al., 2009). In Atlantic salmon, higher Se levels (at least 15 mg/kg in diet) can lead to oxidative stress and change the lipid metabolism of organic and inorganic Se (Berntssen et al., 2017). In addition, in Acipenser sturgeon (Acipenser transmontanus), excessive Se in the diet leads to vacuolar degeneration of cells and necrosis of the liver (Tashjian et al., 2006). In a word, the mechanism of the negative effect of high Se intake on the antioxidant system of aquatic animals is still unclear.
4.2 Harmful effects of Se deficiency
The necessity and demand for dietary Se have been estimated in various fish (Khan et al., 2017). Although Se poisoning may cause multiple damages to fish, the effect of dietary Se deficiency in fish cannot be ignored. It has been reported that Se deficiency is closely related to the occurrence of many diseases in aquatic animals and the impairment of physiological functions under various conditions (Zheng et al., 2018; Wang et al., 2018). Se deficiency can inhibit organs growth and reduce immune functions, thus leading to many inflammatory diseases (Zheng et al., 2018; Hofstee et al., 2017). Se has been proved to be a protective trace element in the liver of many animals. Se deficiency can lead to immune deficiency, inhibit fish growth and induce oxidative stress in the liver (Zheng et al., 2018; Byron and Santolo, 2018). Oxidative stress can stimulate liver inflammation, thereby aggravating liver injury (Mukhopadhyay et al., 2018). In a research on the mechanism of carp liver inflammation, dietary Se deficiency can lead to Se deficiency in blood and liver, leading to overexpression of heat shock protein HSP60 in the liver, aggravating and forming inflammatory damage to the liver (Gao et al., 2019). Se deficiency also impairs the structural integrity of the head kidney, spleen and skin of juvenile grass carp, leads to oxidative damage and aggravating cell apoptosis due to downregulate the activities of antioxidant enzymes (SOD, CAT, GPX, GSTR, and GR) and the mRNA levels related to the signal transduction part (Zheng et al., 2018).
5 Effects of Se-rich fish on humans
Food is the main source of Se intake by the human. As like fish, Se is mainly involved in regulating human various physiological activities in the form of selenoproteins. Se deficiency or Se excess can have adverse effects on the human (Rayman, 2008). Fish is a kind of food with the highest natural Se content and tender flesh, rich in mineral elements, proteins and vitamins, which is the preferred ingredient for people to supplement trace elements through diet. Fish reared in a Se-rich water environment and fed with Se-rich feed can be processed and prepared into bioactive peptide foods such as fish collagen peptides. Eating Se-rich bioactive peptide foods can improve the absorption rate of Se in the body and Se supplement is more efficient (Xia et al., 2022).
Se can reduce the incidence rate of heart disease in humans, but ROS formed during oxidative stress can initiate lipid peroxidation, damage normal cell function, and lead to myocardial ischemia reperfusion (I/R) injury. Se enzyme and the whole thioredoxin system are directly reduce the content of lipid peroxide, protect vascular endothelial cells from oxidative damage, and inhibit Low Density Lipoprotein (LDL) oxidation (Furman et al., 2004; Venardos and Kaye, 2007). SELENOM may be able to alleviate disorders of lipid metabolism and high-fat diet (HFD)-mediated mitochondrial damage in NAFLD. SELENOM regulates Parkin-mediated mitophagy via the AMPKα1–MFN2 signaling pathway, blockade of the AMPKα1–MFN2 pathway and inhibit mitophagy. Moreover, SELENOM deletion inhibits the expression of FAO-related genes (Ppara, Cpt1α, Cdh15, Acox1 and Acadm), and increases the expression of lipogenic genes (Gpam, Plin1, Scd1, Lipe, Fasn, Acly, and Pparg) (Cai et al., 2022). It has been shown that during wound healing some selenoproteins (GPX, SELENOS and SELENOP) bind together with produce effects in the inflammatory phase, such as antioxidant, inhibition of inflammatory cytokines, scavenging of peroxynitrite and enhancing immune function by increasing the survival of phagocytes during phagocytosis (Lei et al., 2009). Se is play a key role in reducing and preventing cancer caused by several carcinogens and inducing apoptosis of cancer cells (Tinggi, 2008). Se level is negatively correlated with human cancer risk. Genomic studies and animal models have indicated that Se intake influences the expression of selenoprotein genes and pathways key to colorectal carcinogenesis such as the antioxidant response, immune and inflammatory pathways (including NF-kB and Nrf2 signaling), the Wnt signaling pathway, protein synthesis pathway (Ye et al., 2021). Se also reduces the incidence of autoimmune thyroiditis and other related conditions, and the reduction of thyroid autoimmune effects is related to the role of GPX and thioredoxin reductase (TrxR) as antioxidant defense systems that scavenge ROS and excess H2O2 produced by thyroid cells during thyroid hormone synthesis, which can lead to thyroid cell necrosis and increased macrophage invasion in severe nutritional Se deficiency (Duntas, 2006).
6 Antioxidant mechanism of different Se forms in fish
In the intensive aquaculture system, cultured fish mainly obtain the selenium from the feed. There are three main forms of selenium additives: one is inorganic Se, which enters animals through passive diffusion in the form of Se4+, and is quickly reduced to selenides (H2Se) in the intestine; the second is organic Se, which is actively absorbed by fish in the form of amino acids, combines with plasma protein to form SeMet; the third is Nano-Se can activate Nrf2 signal transduction pathway to express genes related to antioxidant enzymes. No matter inorganic Se, organic Se or Nano-Se, it will be converted into selenoproteins to play a role after being absorbed by fish. Selenoproteins related to fish antioxidant mechanism include GPXs, TXNRDs, SELENOP, SELENOS, and other selenoproteins, which regulate lipid metabolism, inflammatory damage, ROS and H2O2 formation oxidative stress through antioxidant enzymes (SOD, GPX, and CAT) in fish antioxidant system. In addition, the regulation of selenium deficiency in the human antioxidant system will cause diseases of the heart system, immune system and thyroid function damage (Yu et al., 2020; Wischhusen et al., 2019) (Figure 1).
FIGURE 1. Antioxidant mechanism of different Se forms in fish. Nano-Se, Nano-Selenium; Organic Se, Organic Selenium; Inorganic Se, Inorganic Selenium; GPXs, glutathione peroxidase family; TXNRDs, thioredoxin reductase family.
7 Conclusion
In summary, Se is an essential mineral element for antioxidant stress of aquatic animals and plays an important role in the antioxidant system of aquaculture. We can further study the most effective form of Se in the antioxidant system of aquatic animals, selectively prevent the oxidative stress of aquaculture animals, clarify the mechanism of selenoproteins in the antioxidant system of aquatic animals, and provide direction for the study of Se toxicity. Due to the various functions of selenoproteins, the mechanism of specific selenoprotein function and expression can be considered to prevent the oxidation state of aquatic animals. In the future, we can also compare the effects of Se on other organisms and study the mechanism of Se on the antioxidant system of aquatic animals. This will provide important information for the extensive application of antioxidant systems in aquaculture. This will provide important information for the extensive application of antioxidant systems in aquaculture.
Author contributions
Conceptualization, Z-ML and L-SW; methodology, J-QH; software, Z-ML validation, Z-ML, X-MJ, and L-SW; formal analysis, Z-ML; investigation, Z-ML; resources, J-QH; data curation, Z-ML; writing—original draft preparation, Z-ML; writing—review and editing, Z-ML, JQH, and L-SW; visualization, X-MJ; supervision, L-SW; project administration, L-SW; funding acquisition, L-SW. All authors have read and agreed to the published version of the manuscript.
Funding
This research was funded by Innovation Team Project of Dalian Ocean University, China (B202102) and the Central Guidance on Local Science and Technology Development Fund of Hebei Province (226Z7103G), China.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
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Keywords: selenium, aquatic animals, antioxidant, oxidative stress, selenoprotein
Citation: Li Z-M, Wang X-L, Jin X-M, Huang J-Q and Wang L-S (2023) The effect of selenium on antioxidant system in aquaculture animals. Front. Physiol. 14:1153511. doi: 10.3389/fphys.2023.1153511
Received: 29 January 2023; Accepted: 13 February 2023;
Published: 26 April 2023.
Edited by:
Zhen Zhang, Feed Research Institute (CAAS), ChinaReviewed by:
Ziwei Zhang, Northeast Agricultural University, ChinaBin Feng, Sichuan Agricultural University, China
Copyright © 2023 Li, Wang, Jin, Huang and Wang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Lian-Shun Wang, wanglianshun@dlou.edu.cn