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Growth, serum biochemical parameters, salinity tolerance and antioxidant enzyme activity of rainbow trout (Oncorhynchus mykiss) in response to dietary taurine levels

  • Corresponding author: Yangen Zhou, zhouyg@ouc.edu.cn
  • Received Date: 2020-08-07
    Accepted Date: 2020-12-04
    Published online: 2021-02-19
  • Edited by Xin Yu.
  • This study evaluated the effect of dietary taurine levels on growth, serum biochemical parameters, salinity adaptability, and antioxidant activity of rainbow trout (Oncorhynchus mykiss). Four diets were formulated with taurine supplements at 0, 0.5, 1, and 2% w/v (abbreviated as T0, T0.5, T1, and T2, respectively). Rainbow trouts (initial weight of 80.09 ± 4.72 g) were stocked in tanks (180 L capacity), and were fed these diets for six weeks and subsequently underwent salinity acclimation. Physiological indicators were determined before salinity acclimation at 1, 4, 7, and 14 days afterwards. Results showed that there were no significant differences in growth performance (final mean weight ranged from 182.35 g to 198.48 g; percent weight gain was between 127.68% and 147.92%) of rainbow trout in freshwater stage, but dietary taurine supplement significantly increased serum-free taurine content. After entering seawater, the Na+-K+-ATPase activity of T2 group returned to its freshwater levels, and the serum cortisol content was significantly higher than T0 and T0.5 groups. At the end of this experiment, the liver superoxide dismutase activity in the T0 and T0.5 groups was significantly lower than in the T1 and T2 groups, and the liver catalase in the T0 group was the lowest whereas that in the T2 group was the highest. Muscle malondialdehyde content was the highest in the T0 group, and the lowest in the T2 group. Based on the results of this study, supplement of dietary taurine (0.5-2%) enhanced the salinity tolerance in rainbow trout, which increased with the higher taurine concentration.
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Growth, serum biochemical parameters, salinity tolerance and antioxidant enzyme activity of rainbow trout (Oncorhynchus mykiss) in response to dietary taurine levels

    Corresponding author: Yangen Zhou, zhouyg@ouc.edu.cn
  • 1. Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao 266003, China
  • 2. School of Fisheries, Aquaculture, and Aquatic Sciences, Auburn University, Auburn, AL 36849-54119, USA
  • 3. Function Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology, Qingdao 266235, China

Abstract: This study evaluated the effect of dietary taurine levels on growth, serum biochemical parameters, salinity adaptability, and antioxidant activity of rainbow trout (Oncorhynchus mykiss). Four diets were formulated with taurine supplements at 0, 0.5, 1, and 2% w/v (abbreviated as T0, T0.5, T1, and T2, respectively). Rainbow trouts (initial weight of 80.09 ± 4.72 g) were stocked in tanks (180 L capacity), and were fed these diets for six weeks and subsequently underwent salinity acclimation. Physiological indicators were determined before salinity acclimation at 1, 4, 7, and 14 days afterwards. Results showed that there were no significant differences in growth performance (final mean weight ranged from 182.35 g to 198.48 g; percent weight gain was between 127.68% and 147.92%) of rainbow trout in freshwater stage, but dietary taurine supplement significantly increased serum-free taurine content. After entering seawater, the Na+-K+-ATPase activity of T2 group returned to its freshwater levels, and the serum cortisol content was significantly higher than T0 and T0.5 groups. At the end of this experiment, the liver superoxide dismutase activity in the T0 and T0.5 groups was significantly lower than in the T1 and T2 groups, and the liver catalase in the T0 group was the lowest whereas that in the T2 group was the highest. Muscle malondialdehyde content was the highest in the T0 group, and the lowest in the T2 group. Based on the results of this study, supplement of dietary taurine (0.5-2%) enhanced the salinity tolerance in rainbow trout, which increased with the higher taurine concentration.

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Introduction
  • According to a report of the Food and Agriculture Organization of the United Nations (FAO), salmonids have become the world's third-largest group of farmed fish, and more than two million tonnes are produced annually (Pauly and Zeller 2017). The salmon market is growing rapidly in China with increasing demand; however, it still largely relies on imports. Chinese researchers and entrepreneurs have attempted to culture salmonids in open sea areas, such as Qingdao, Yantai, and Dalian, since the 1970s, but have not had any success because of the high water temperature in summer (Dong 2019). However, a huge large cold-water mass exists in the Yellow Sea, where the water condition has proved to be suitable for salmonid farming (Dong 2015; Han et al. 2016). Thus, Chinese researchers and entrepreneurs have started carrying out offshore salmonid mariculture with deep-sea fish farming facilities in this area, and the first successful attempt was made in January 2019 (Dong 2019; Evans 2018). The main farmed species include Atlantic salmon (Salmo salar) and rainbow and steelhead trout (Oncorhynchus mykiss).

    Rainbow trout is one of the most widely cultivated cold-water fish species in China (Zhao et al. 2019), but it is mainly cultured in freshwater plateau reservoirs and mountain areas. However, previous studies reported that mariculture may improve the growth performance, disease resistance, and flavor of rainbow trout (Shepherd et al. 2005; Thorarensen et al. 1996; Yada et al. 2001). Therefore, salinity acclimation and mariculture may be a promising way to improve the quality of this fish.

    The salinity tolerance of rainbow trout is affected by many factors, such as age, size, salinity stimulation, photoperiod, temperature, and nutrients during smoltification (Bjerknes et al. 1992; Brown et al. 2018; Handeland et al. 2013; Morgan and Iwama 1991; NRC 2011; Strand et al. 2018). Amino acids, that play vital roles in salinity adaptability of fish, include arginine, histidine, alanine, aspartic acid, glycine, serine and taurine (Aragao et al. 2010; Hosoi et al. 2008; Li et al. 2009; Salze and Davis 2015). Furthermore, Aragao et al. (2010) reported that non-essential amino acids (NEAA) are more important than essential amino acids (EAA) in osmoregulation of fish.

    After transferring fish to a hypertonic environment, the biochemical homeostasis of the cell membrane is disrupted by salinity stress, generating numerous reactive oxygen species (ROS). Thus, antioxidant enzymes, such as catalase (CAT) and superoxide dismutase (SOD), are mobilized to maintain homeostasis (Abdel-Tawwab and Monier 2018; De Mercado et al. 2018; Flohr et al. 2012; Lopes et al. 2013; Suji and Sivakami 2008; Wang et al. 2016). The antioxidant activity was easily affected by dietary components, including lipid sources (Tan et al. 2017; Zuo et al. 2012), vitamins (Chen et al. 2013) and taurine (Bañuelos-Vargas et al. 2014).

    Taurine is a conditional amino acid in many fish species, and dietary supplements have positive effects on rainbow trout (NRC 2011). Taurine exerts an important role in osmoregulation of fish (HuxTable 1992; Lambert et al. 2015; Schaffer et al. 2000; Takagi et al. 2011), and it is the major free amino acid balancing osmotic pressure in larval freshwater fish (Zhang et al. 2006).

    The advantages of taurine on osmoregulation of fish may lie in three areas: (1) taurine acts as an organic osmolyte, maintaining cell osmolality and volume (Yancey 2001a, b); (2) due to the abundance of taurine, EAA are more likely to be used in the synthesis of stress-related proteins than in organic osmolytes or energy supply (Aragao et al. 2010; Wilson 2003); (3) taurine promotes the function of the antioxidant system (Salze and Davis 2015) and helps fish cope with salinity stress.

    With the development of nutritional research, "functional aquafeeds" and "environmentally oriented aquafeeds" are getting more attention. Environmentally oriented aquafeeds function to alleviate negative influences in fish caused by external changes (including temperature, salinity, stressors and ammonia) (Li et al. 2009). Under stressful conditions, fish have extra amino acid requirements, to meet increased energy requirements or for the synthesis of proteins related to handling stress (Aragao et al. 2008; Costas et al. 2008; Pinto et al. 2007). The taurine demand of rainbow trout during salinity acclimation may be higher than that in the freshwater stage. Therefore, this study investigated the effect of dietary supplements of taurine at different concentrations (0, 0.5, 1, and 2%) on growth, serum biochemical parameters, salinity tolerance, and antioxidant activity of rainbow trout.

Results

    Growth of rainbow trout

  • At the end of the 6-week period, no significant differences were observed in rainbow trout survival rate (91.67-100%), final mean weight (182.35-198.49 g), final biomass (2013.45-2381.93 g), percent weight gain (127.68-147.92%), thermal-unit growth coefficient (TGC) (0.19-0.21), and feed conversion ratio (FCR) (1.20-1.68) (Table 1).

    Parameters T0 T0.5 T1 T2 PSE P value
    Final mean weight (g) 188.27 195.45 198.49 182.35 9.1481 0.6159
    Final biomass (g) 2259.25 2345.38 2381.93 2013.45 153.8494 0.3823
    Percent weight gain (%) 134.92 144.14 147.92 127.68 11.4407 0.6117
    Survival (%) 100 100 100 91.67 4.1667 0.4411
    FCR 1.68 1.2 1.29 1.67 0.1942 0.2499
    TGC 0.2 0.21 0.21 0.19 0.0136 0.6698
    Values are the means of three replicates. Significant differences (P < 0.05) were determined using one-way ANOVA following by the Student–Newman–Keuls (SNK) test
    PSE pooled standard error, FCR feed conversion ratio, TGC thermal growth coefficient

    Table 1.  Growth performance of rainbow trout fed four experimental diets for six weeks (initial weight, 80.09 ± 4.72 g, n = 3)

  • Serum biochemical parameters of rainbow trout during salinity acclimation

  • No significant differences were detected in serum total protein (TP) and albumin (ALB) content of rainbow trout before salinity acclimation (Fig. 1a, b). The serum TP content in the T0 group significantly decreased on day 7 after salinity acclimation, and the TP content in the T0 group was significantly lower compared to other groups. There was no significant change in the ALB content in the T2 group during salinity acclimation. However, the ALB content in the T0, T0.5, and T1 groups decreased on day 7, and was significantly lower than their freshwater values. On day 14, the ALB content in the T0.5 and T1 groups returned to their freshwater values, whereas the ALB content in the T0 group was still significantly lower than its freshwater value and the values in the other groups.

    Figure 1.  Variations in the serum TP (a) and ALB (b) contents of rainbow trout fed different dietary taurine levels during salinity acclimation. Note: TP total protein, ALB albumin. Values are the means of three replicates. Different capital letters indicate significant differences (P < 0.05) at different times in the same dietary treatment, and different lowercase letters indicate significant differences (P < 0.05) among different dietary treatments at the same time based on one-way ANOVA following by the Student-Newman-Keuls (SNK) test. FW-42: end of growth experiment. SW-1: one day after salinity reached 30. SW-4: four days after salinity reached 30. SW-7: seven days after salinity reached 30. SW-14: fourteen days after salinity reached 30

    Before salinity acclimation, the serum lactate dehydrogenase (LDH) content of rainbow trout in the T0 and T0.5 groups was higher than that in the T1 and T2 groups (Fig. 2a). The LDH content in all groups increased significantly on day 1 after salinity acclimation, and decreased to their freshwater values on day 4. There was no significant difference in alkaline phosphatase (ALP) content among different groups before salinity acclimation (Fig. 2b). The ALP content in the T0 and T0.5 groups increased significantly after salinity acclimation and returned to their freshwater values on day 7. On day 14, the ALP content in the T0 and T0.5 groups was significantly lower than their freshwater values and the values in the T1 and T2 groups. The alanine transaminase (ALT) content of trout in the T1 and T2 groups was significantly higher compared to that in the T0 and T0.5 groups before salinity acclimation (Fig. 2c). The ALT content in the T0, T0.5, and T1 groups increased significantly on day 1 after acclimation. Moreover, the ALP content of trout in all groups increased significantly on day 7 after experiencing a significant decrease on day 4 after salinity acclimation. On day 14, the ALT content returned to its freshwater value only in the T2 group, but not in others. Thus, the ALT content in the T0, T0.5, and T1 groups was significantly lower than in the T2 group on day 14. Moreover, no significant difference of aspartate transaminase (AST) was observed among groups before salinity acclimation (Fig. 2d). The AST content was steady in the T0 group but fluctuated in the other groups. On day 14, the AST content in the T0 group was significantly lower than its freshwater value, and the AST content in the T2 group was significantly higher than in the other groups.

    Figure 2.  Variations in the serum LDH (a), ALP (b), ALT (c), AST (d) contents of rainbow trout fed different levels of dietary taurine during salinity acclimation. Note: LDH lactate dehydrogenase, ALP alkaline phosphatase, ALT alanine transaminase AST aspartate transaminase. Same as those of Fig. 1

    No significant difference was observed in rainbow trout serum glucose (GLUC) and cholesterol (CHO) content between groups before salinity acclimation, whereas the serum triglyceride (TRIGL) content of trout in the T1 group was significantly higher compared to that in the other groups (Fig. 3a-c). On day 1 after salinity acclimation, the mean values of serum GLUC decreased in all groups, and then fluctuated (the difference was not significant due to the large individual difference). The serum TRIGL content decreased significantly in all groups after salinity acclimation. On day 14, the mean values of GLUC, TRIGL, and CHO content in the T0 group were lower than in the other groups.

    Figure 3.  Variations in the serum GLUC (a), CHO (b), and TRIGL (c) contents of rainbow trout fed different levels of dietary taurine during salinity acclimation. Note: GLUC: glucose; TRIGL: triglyceride; CHO: cholesterol. Same as those of Fig. 1

    During salinity acclimation, significant effect of interactions of dietary taurine levels and time were observed on serum TP [Student-Newman-Keuls (SNK), P = 0.0301], ALB (P = 0.0015), LDH (P = 0.0022), ALP (P < 0.0001), ALT (P < 0.0001), AST (P < 0.0001), GLUC (P = 0.0228), and TRIGL (P = 0 0.0174) in rainbow trout (Table 2).

    Parameters Model Time Level Time × Level
    TP (g/L) 0.0004 0.0002 0.0222 0.0301
    ALB (g/L) < 0.0001 < 0.0001 < 0.0001 0.0015
    LDH (U/L) < 0.0001 < 0.0001 0.0077 0.0022
    ALP (U/L) < 0.0001 < 0.0001 0.3551 < 0.0001
    ALT (U/L) < 0.0001 < 0.0001 0.0136 < 0.0001
    AST (U/L) < 0.0001 < 0.0001 0.596 < 0.0001
    GLUC (mmol/L) 0.0002 < 0.0001 0.0808 0.0228
    TRIGL (mmol/L) < 0.0001 < 0.0001 0.003 0.0174
    CHO (mmol/L) 0.0976 0.0024 0.7287 0.6477
    TP total protein, ALB albumin, LDH lactate dehydrogenase, ALP alkaline phosphatase, ALT alanine transaminase, AST aspartate transaminase, GLUC glucose, TRIGL triglyceride, CHO cholesterol

    Table 2.  P value of two-way ANOVAs for the effects of time and dietary taurine contents on the serum TP, ALB, LDH, ALP, ALT, AST, GLUC, TRIGL, and CHO contents

  • Osmoregulation of rainbow trout during salinity acclimation

  • Before salinity acclimation, the serum osmolality of rainbow trout in the T0 group was significantly lower than in the other groups (Fig. 4a). The serum osmolality of trout in the T1 group increased temporarily after salinity acclimation, and it returned to its freshwater value on day 4.

    Figure 4.  Variations in the serum osmolality (a), serum Na+ (b), serum K+ (c), serum Ca2+ (d), serum Mg2+ (e), serum Cl (f) of rainbow trout fed different levels of dietary taurine during salinity acclimation. Note: Same as those of Fig. 1

    No significant differences of serum concentrations of Ca2+, Mg2+, Na+, K+, and Cl in rainbow trout were observed before salinity acclimation (Fig. 4b-f). The serum Mg2+ content in the T0 group was constant after salinity acclimation, whereas the Mg2+ concentration in the T0.5, T1, and T2 groups fluctuated, and returned to their freshwater values on day 7, after showing a trend from increase to decline. After exposure to seawater, the serum Na+ and Cl concentrations increased significantly. On day 4, the serum Cl concentration in the T0 group was significantly higher than in the T0.5 and T1 groups. After salinity acclimation, the serum K+ concentration in all groups decreased. The serum K+ concentration in the T1 and T2 groups was significantly higher compared to that in the T0 and T0.5 groups on days 4 and 7. There was no significant difference in K+ concentration between groups on day 14.

    There was no significant difference in rainbow trout gill Na+-K+-ATPase (NKA) before salinity acclimation (Fig. 5a). Salinity stress significantly inhibited gill NKA activity in all groups on day 1 after acclimation. The gill NKA activity of trout in the T2 group returned to its freshwater value on day 7, whereas the gill NKA activity in the T0, T0.5, and T1 groups failed to recover to their freshwater values until the end of the salinity acclimation experiment. On days 4 and 14 after salinity acclimation, the gill NKA activity in the T2 group was significantly higher than in the other groups. No significant difference in serum cortisol concentration was observed among groups before salinity acclimation (Fig. 5b). After exposure to the seawater, the serum cortisol concentrations of trout in the T0 and T0.5 groups decreased to the lowest values on days 7 and 4, respectively, and then increased. The serum cortisol concentrations of trout in the T1 and T2 groups were steady after acclimation. On day 14, the serum cortisol concentrations of trout in the T1 and T2 groups were significantly higher compared to that in the T0 and T0.5 groups.

    Figure 5.  Variations in the gill NKA activity (a) and serum cortisol concentration (b) of rainbow trout fed different levels of dietary taurine during salinity acclimation. Note: NKA: Na+, K+-ATPase. Same as those of Fig. 1

    During the salinity acclimation, significant effect of interactions of dietary taurine levels and time were observed on rainbow trout serum K+ concentration (P = 0.0016), Mg2+ concentration (P = 0.0042), and cortisol (P < 0.0001) (Table 3).

    Parameters Model Time Level Time × Level
    Osmolality (mOsm/kg) 0.003 0.0005 0.0522 0.1186
    Na+ (mmol/L) < 0.0001 < 0.0001 0.8825 0.5281
    K+ (mmol/L) < 0.0001 < 0.0001 < 0.0001 0.0016
    Ca2+ (mmol/L) 0.0114 0.0052 0.3119 0.0546
    Mg2+ (mmol/L) < 0.0001 < 0.0001 0.2779 0.0042
    Cl (mmol/L) < 0.0001 < 0.0001 0.6748 0.0816
    NKA (μmolPi/(mg·h) prot) < 0.0001 < 0.0001 < 0.0001 0.1438
    Cortisol (Pg/ml) < 0.0001 < 0.0001 < 0.0001 < 0.0001
    NKA: Na+, K+-ATPase

    Table 3.  P value of two-way ANOVAs for the effects of time and dietary taurine contents on the serum osmolality, serum ion concentration, serum cortisol contents, and gill NKA activity of rainbow trout during salinity acclimation

  • Antioxidant activity of rainbow trout during salinity acclimation

  • No significant differences in liver SOD and CAT activity were observed among treatment groups before salinity acclimation (Fig. 6a, b). The SOD activity of trout in the T0 group decreased continually after acclimation. The SOD activity in the T0.5, T1, and T2 groups decreased significantly on day 1 after acclimation and returned to their freshwater values on day 4. However, the SOD activity in the T0.5 and T1 groups decreased significantly again on days 7 and 14, respectively. At the end of the salinity acclimation experiment, SOD activity in the T0 and T0.5 groups was significantly lower than that in the T1 and T2 groups. After salinity acclimation, liver CAT activity fluctuated, and the CAT activity in the T0 group was significantly lower than in the other groups on day 14.

    Figure 6.  Variations in the liver SOD activity (a), liver CAT activity (b) and muscle MDA concentration (c) of rainbow trout fed different levels of dietary taurine during salinity acclimation. Note: SOD superoxide dismutase, CAT catalase, MDA malondialdehyde. Same as those of Fig. 1

    Before salinity acclimation, there was no significant difference in muscle malondialdehyde (MDA) content of rainbow trout (Fig. 6c). The muscle MDA content in the T0.5, T1, and T2 groups increased significantly on day 1 after acclimation, and decreased continually on days 4 and 7. At the end of the salinity acclimation experiment, the muscle MDA content was the highest in the T0 group, and the lowest in the T2 group.

    During salinity acclimation, significant effects of interactions of dietary taurine levels and time were observed on rainbow trout liver SOD activity (P < 0.0001) and CAT activity (P = 0.0003) (Table 4).

    Variable SOD
    (U/mg prot)
    CAT
    (U/mg prot)
    MDA
    (nmol/mg prot)
    Model < 0.0001 < 0.0001 < 0.0001
    Time < 0.0001 < 0.0001 < 0.0001
    Level < 0.0001 0.0002 0.0135
    Time × Level < 0.0001 0.0003 0.4538
    SOD superoxide dismutase, CAT catalase, MDA malondialdehyde

    Table 4.  P value of two-way ANOVAs for the effects of time and dietary taurine contents on the liver SOD activity, liver CAT activity and muscle MDA concentration

  • Serum-free amino acids of rainbow trout before and after salinity acclimation

  • The effect of dietary taurine content on serum-free amino acids of rainbow trout is shown in Fig. 7. The serum-free glycine and alanine contents were lower in the T0 group compared to that in the other groups during the freshwater stage, and the serum-free proline content in the T2 group was lower than in the other groups on day 14 after salinity acclimation. Serum-free taurine of rainbow trout was positively correlated with dietary taurine content in both freshwater and seawater. The comparison of serum-free taurine content before and after salinity acclimation of rainbow trout is presented in Fig. 8. After salinity acclimation, the serum-free taurine content decreased significantly in the T0 group, and increased significantly in the T2 group. In addition, no significant difference in serum taurine content was observed in the T0.5 and T1 groups before and after salinity acclimation.

    Figure 7.  Serum free amino acid of rainbow trout in different dietary groups before (a) and after salinity acclimation (b). Note: Same as those of Fig. 1

    Figure 8.  Comparison of the serum-free taurine content of rainbow trout in different dietary groups before and after salinity acclimation. Note: values are the means of three replicates. Stars (*) denote a significant difference (P < 0.05) based on a t-test. FW-42: end of growth experiment. SW-14: fourteen days after salinity reached 30

Discussion

    Effect of dietary taurine content on growth of rainbow trout

  • Although rainbow trouts are able to biosynthesize taurine even at the juvenile stage, the level of biosynthesis is insufficient, and therefore dietary sources containing taurine are necessary (Wang et al. 2015). Although dietary taurine is known to have positive effects on rainbow trout growth, the level of taurine requirement is still unclear (NRC 2011). In the present study, no significant difference in growth performance was observed between rainbow trout groups fed diets with different levels of dietary taurine for six weeks. These results indicate that the rainbow trout taurine demand may be met by 30% fish meal diet (containing 0.18% taurine). Similarly, Gaylord et al. (2006) reported that dietary taurine improved rainbow trout growth only when an all-plant protein diet was provided.

  • Effect of dietary taurine content on serum biochemical parameters of rainbow trout

  • Serum biochemical parameters are important indicators of fish physiological stress (Lermen et al. 2004), and may be used to promote fish health management (Chen et al. 2004). Serum TP content is an important non-specific immune parameter, often used as a basic indicator of fish health (Adham et al. 1997; Adhikari et al. 2004). Our finding showed that the serum TP content of rainbow trout in the T0 group decreased after salinity acclimation, and was significantly lower than in the other groups. It is possible that the protein biosynthesis of rainbow trout in the T0 group was inhibited, or the biosynthesized proteins were utilized for metabolic purposes (e.g., energy supply) (Mc Donald and Milligan 1992; Priya et al. 2012). Serum ALB content may reveal general nutritional status, liver function, and the integrity of the vascular system of fish. Also, it exerts a role in some important metabolic processes and the transport of substances (especially lipids) (Andreeva 2010; Priya et al. 2012). Our results showed that the ALB content of trout in the T0 group significantly decreased on day 14 after salinity acclimation, and was lower than ALB content in freshwater and in the other groups. This may indicate that the process of metabolism and transport in trout in this group was impaired to some extent.

    LDH, ALP, ALT, and AST are indispensable enzymes in maintaining basic physiological functions in fish (Fazlolahzadeh et al. 2011). LDH catalyzes the interconversion of pyruvate and lactate during glycolysis and gluconeogenesis, increasing LDH content indicated organ damage (Armstrong et al. 2012; Feron 2009). ALP is a multifunctional enzyme that functions as a transphosphorylase at alkaline pH. Moreover, ALP is essential for the mineralization of the skeleton in aquatic animals (Lan et al. 1995; Zikic et al. 2001). AST and ALT are two major aminotransferases, which are involved in protein and amino acid metabolism (Folmar 1993; Zikic et al. 2001). In the current study, the serum ALT content in all trout groups and the serum ALP content in trout in the T0 and T0.5 groups increased significantly after salinity acclimation. Our results may indicate damage of some trout organs due to salinity stress because the elevation of serum ALP, ALT, and AST generally indicates damage and dysfunction of the liver, kidney, and gill in fish (Bernet et al. 2001; Liu et al. 2020; Nemcsok and Benedeczky 1995). Additionally, Oner et al. (2008) reported that the decrease in serum ALP content was related to cell membrane transport system disorder. Thus, the recovery of ALT and AST content in trout only occurred in the T2 group whereas the ALP, ALT, and AST contents in the T0 and T0.5 groups were significantly lower than in the T2 group at the end of the salinity acclimation experiment. This may indicate organ dysfunction in trout in the T0 and T0.5 groups.

    Acclimation to environmental stress in fish requires energy supply, and the oxidation of GLUC and TRIGL is energy source derived from metabolism (Cho et al. 2015; Liu et al. 2020). Our results showed that in rainbow trout, serum TRIGL content decreased significantly, and the GLUC content dramatically fluctuated after salinity acclimation. This indicates a stronger energy demand in trout for adaptation to a hypertonic environment. On day 14 after acclimation, the mean TRIGL content in the T0 group was lower than that in the other groups, which may imply that the fishes in this group were more stressed, and had a greater energy demand.

  • Effect of dietary taurine content on rainbow trout osmoregulation

  • Salinity adaptability in fish depends on its capacity to regulate the ion uptake and excretion, and maintain a relatively steady osmolality (Zhao et al. 2011). Failure to regulate ion concentrations in blood results in reduced cellular excitability, disrupted membrane potential and cell death (Holmes and Donaldson 1969). In general, the acclimation process of euryhaline fish transferred from freshwater to seawater may be divided into two stages: the critical stage (rapidly changing osmotic parameters) and the chronic or regulatory stage (newly established homeostasis in osmotic parameters) (Holmes and Donaldson 1969; Zhao et al. 2011). In the current study, no significant fluctuation in trout serum Na+, Ca2+, and Cl concentrations was observed during salinity acclimation, which indicated that rainbow trout may successfully adapt to the seawater environment by gradual acclimation (3 g/L per day). According to Soegianto et al. (2017), fish serum ion concentration changes in different salinities; serum Ca2+, Na+, and Cl were higher in hypertonic environments compared to those in hypotonic environments. Similarly, our findings showed that trout serum Na+ and Cl concentrations significantly increased after salinity acclimation because of the influence of the high concentrations of Na+ and Cl in seawater. In addition, our results showed a significant decrease in serum K+ concentration after salinity acclimation. This is in agreement with the results of Soegiantoet al. (2017), who reported a lower serum K+ concentration in East Java strain tilapia (Oreochromis niloticus) exposed to hypertonic environments (10 and 15 g/L salinity) compared to hypotonic environment (0 and 5 g/L salinity). The decrease in serum K+ concentration may be related to osmotic adaptation: in hyperosmotic environments. Fish gills are permeable to K+ where efflux is greater than influx. Thus, the reduction in K+ concentration in seawater balances the osmotic difference in the intracellular fluid caused by the increase in Na+ and Cl (Nussey et al. 1995; Sanders and Kirschner 1983; Soegianto et al. 2017; Witters 1986).

    After being transferred into hypertonic environments, fishes swallow a lot of seawater to make up for the osmotic water loss across the cell integument. The excess Na+ and Cl- in seawater are removed through chloride cells located in the gill epithelium whereas Ca2+ and K+ are excreted by the kidney (Cataldi et al. 1995; Krayushkina et al. 1995; Soegianto et al. 2017). NKA is the main enzyme in salmonids regulating blood ion gradient and maintaining cell homeostasis (Sakamoto et al. 2001; Vieira et al. 2018). Our results showed that trout gill NKA activity significantly decreased after salinity acclimation, and the recovery to freshwater values only occurred in the T2 group, which may indicate a more efficient osmoregulation ability of trout in the T2 group. This explanation is consistent with Rodriguez et al. (2002), who found that spiral valve NKA activity of Siberian sturgeon (Acipenser baerii) first decreased to diminish the ionic Na+ and Cl inflow, and recovered upon alternation to the new media environment by transferring to salinity of 9-14.

    Cortisol is the main corticosteroid that regulates water balance processes, and stimulates the development of gill chloride cells, enhances the gill NKA activity, and increases the salinity adaptability of fish (Lin et al. 2000; Mancera and McCormick 1999; McCormick et al. 2008; Shaughnessy and McCormick 2018; Singer et al. 2003). Our results showed that serum cortisol content of rainbow trout in the T0 and T0.5 groups was significant on days 4 and 7 after salinity acclimation. Although serum cortisol content in the T0.5 group returned to its freshwater value, the cortisol contents in the T0 and T0.5 groups were still significantly lower than that in the T2 group on day 14. These results indicated that the salinity adaptability of rainbow trout in the T2 group was most effective, whereas the osmoregulation of trout in the T0 and T0.5 groups was inefficient.

  • Effect of dietary taurine content on antioxidant enzyme activity of rainbow trout

  • SOD and CAT are two kinds of antioxidant enzymes. During the ROS-scavenging process, SOD transforms superoxide anion radicals to H2O2, and CAT converts H2O2 to H2O and O2 (Lopes et al. 2013; Meng et al. 2014; Stara et al. 2012).

    In this study, trout liver SOD activity was temporarily inhibited by salinity stress, and its activity increased after the adaptation period. However, the SOD activity in the T0 and T0.5 groups was still significantly lower than that in the T1 and T2 groups on day 14 after salinity acclimation. This indicates the more effective antioxidant capacity of trout in the latter groups. Similarly, salinity stress temporarily inhibited the liver CAT activity. Subsequently, the CAT activity increased to enhance the clearance of superoxide ions, and the activity declined after the new homeostasis was reached. At the end of the experiment, the CAT activity of trout in the T0 group was significantly lower compared to that in the other groups, which implied the lowest antioxidant ability of trout in the T0 group. These findings are in agreement with those of Bañuelos-Vargas et al. (2014), who reported that supplementary dietary taurine significantly enhanced the CAT activity of totoaba (Totoaba macdonaldi).

    MDA is a product of lipid peroxidation, which is caused by the accumulation of superoxide anion radicals. The increase of MDA level resulted in the increase of cell toxicity, accelerating the damage of cells and tissues (Abdel-Tawwab and Monier 2018; Viarengo et al. 1995). Our results showed that muscle MDA content in trout increased on day 1 after salinity acclimation, because the SOD and CAT activity was inhibited in this time, and a large number of superoxide ions could not be removed. Subsequently, the liver SOD and CAT activity recovered, leading to a gradual decline in the muscle MDA content (stabilizing on day 7). On day 14 after salinity acclimation, the muscle MDA content of trout was the highest in the T0 group, and the lowest in the T2 group, which indicated that rainbow trouts in the T2 group were significantly healthier compared to those in the other groups, and fishes in the T0 group were the least healthy.

  • Effect of dietary taurine content on serum-free amino acids of rainbow trout

  • Osmotic pressure in euryhaline teleost fish is regulated at nearly constant levels (Yancey 2001a). Marine fish depends on the utilization of organic osmolytes rather than inorganic ions to maintain cell osmolality and volume in the long term (Yancey 2001b). These organic osmolytes are essentially nitrogen-based compounds, including several amino acids (Yancey 2001a). NEAA seem to be preferentially used for fish osmoregulation, rather than EAA, as fish cannot synthesize them (Aragao et al. 2010; Wilson 2003).

    In our results, the serum-free taurine content of rainbow trout increased significantly with the increase of dietary taurine supplement. Similarly, Qi et al. (2012) and Gaylord et al. (2007) reported a positive correlation between dietary taurine and taurine content in fish serum and organs. The increase of taurine content improves the osmotic pressure of cells and the antioxidant capacity, which was beneficial for rainbow trout to adapt to the seawater environment and to maintain normal cell function. The serum taurine content of trout in the T2 group increased significantly after salinity acclimation, which may suggest that the salinity adaptability of trout in the T2 group was the most efficient.

    Before salinity acclimation, the glycine and alanine content in the T0 group was significantly lower than that in other groups, whereas the mean values of glycine and alanine content in the T0 group exceeded those in other groups after acclimation. This result may indicate that in the case of taurine deficiency, other amino acids are retained for osmoregulation in rainbow trout, thereby reducing the synthesis efficiency of some important stress-related proteins and further reducing the trout's adaptability to salinity.

Conclusion
  • In summary, our data showed that supplement of dietary taurine did not significantly influence the growth performance of rainbow trout when the feed contained 30% fish meal. However, supplement of dietary taurine significantly improved serum taurine content, which was beneficial for trout to maintain osmolality upon exposure to the seawater. Also, supplement of dietary taurine improved the oxidant capacity of rainbow trout by enhancing the liver CAT and SOD activity and reducing the muscle MDA content. In addition, the salinity adaptability of rainbow trout could be enhanced by supplementing dietary taurine, which increased gill NKA activity and serum cortisol concentration. Based on the results of our study, supplement of dietary taurine may improve the physiological state of rainbow trout during salinity acclimation, where larger supplement concentrations may have more obvious effect.

Materials and methods

    Experimental diets

  • The experimental diet was isoproteic (45% protein) and isolipidic (16% lipid). Fish meal, soybean meal, corn gluten meal and wheat gluten meal were used as protein sources. Fish oil was used as the lipid source. Four diets were formulated with the supplementation of taurine at 0, 0.5, 1, and 2% w/v (abbreviated as T0, T0.5, T1, and T2, respectively). The total taurine levels for diets T0, T0.5, T1, and T2 were 0.18, 0.69, 1.22 and 2.37% w/v, respectively (Table 5). All ingredients were screened using a 250-μm mesh to remove impurities and to ensure an appropriate small size of the particles, and then mixed with fish oil thoroughly. Hot water was then blended into the mixture to make a stiff dough, which was subsequently pelleted in a feed mill. Then, the diets were dried using an oven (45 ℃) for approximately 10 h to achieve a moisture content of 8-10%. After drying, pellets were kept at − 20 ℃ until use.

    Ingredient (% of diet) T0 T0.5 T1 T2
    Fish meala 30.00 30.00 30.00 30.00
    Soybean meala 22.30 22.30 22.30 22.30
    Corn Gluten meala 15.00 15.00 15.00 15.00
    Wheat gluten meala 8.00 8.00 8.00 8.00
    Menhaden fish oila 11.59 11.59 11.59 11.59
    Soybean Lecithina 1.00 1.00 1.00 1.00
    Corn Starcha 9.81 9.31 8.81 7.81
    Mineral and vitamin premixb 1.00 1.00 1.00 1.00
    Choline chloride 0.50 0.50 0.50 0.50
    Betaine 0.50 0.50 0.50 0.50
    Sodium alginate 0.30 0.30 0.30 0.30
    Taurine 0.00 0.50 1.00 2.00
    Proximate composition (% of diet, as-is)
      Crude protein 45.23 45.11 45.88 45.79
      Total lipid 16.95 17.19 17.61 17.63
      Ash 9.54 9.77 10.01 9.63
      Taurine 0.18 0.69 1.22 2.37
    Mineral premix (mg/kg diet): 10 mg CuSO4·5H2O; 25 mg Na2SeO3 (1%); 50 mg ZnSO4·H2O; 50 mg CoC12·6H2O (1%); 60 mg MnSO4·H2O; 80 mg FeSO4·H2O; 180 mg Ca (IO3)2; 1200 mg MgSO4·7H2O
    aFish meal: crude protein 68.03%, crude lipid 9.12%; Soybean meal: crude protein 41.76%, crude lipid 3.26%; Corn Gluten meal: crude protein 61.10%, crude lipid 2.00%; Wheat gluten meal: crude protein 76.55%, crude lipid 2.11%. All ingredients were obtained from Great Seven Bio-Tech (Qingdao, Shandong, China)
    bVitamin premix (mg/kg diet): 5 mg vitamin D; 10 mg vitamin K; 10 mg vitamin B12; 20 mg vitamin B6; 20 mg folic acid; 25 mg vitamin B1; 32 mg vitamin A; 45 mg vitamin B2; 60 mg pantothenic acid; 60 mg biotin; 200 mg niacin acid; 240 mg α-tocopherol; 800 mg inositol; 2000 mg ascorbic acid

    Table 5.  Composition of four diets (45% protein and 16% lipid) with the supplement of taurine of 0, 0.5, 1, and 2%, respectively

  • Experimental design and sample collection

  • The experiment was carried out at the Key Laboratory of Mariculture, Ocean University of China (Qingdao, China). Juveniles were purchased from Wanzefeng Fishery Company (Rizhao, China). Prior to the experiment, fish were nursed in non-circulating system for 14 days with cylindrical tanks by aerated freshwater at 16 ℃. The tank volume (upper diameter, 0.65 m; lower diameter, 0.60 m; height, 0.60 m) was 180 L. Subsequently, fish (80.09 ± 4.72 g; mean ± standard deviation) that appeared to be healthy and were devoid of any signs of disease were randomly assigned to the four treatment groups and fed T0, T0.5, T1, and T2 diets. Each treatment had three replicate tanks (12 fish per tank). Fish were fed to satiation twice per day by hand (at 8:30 and 16:30 h). Throughout the entire experiment, a 12:12 h light: dark cycle was maintained. Approximately half of water volume was exchanged by hand twice per day at 13:00 h and 21:00 h. The water quality parameters (mean ± standard deviation) were maintained: dissolved oxygen (DO) at 8.76 ± 0.65 mg/L, temperature at 17.1 ± 0.49 ℃, pH at 7.82 ± 0.17, nitrite nitrogen at 0.03 ± 0.01 mg/L, and ammonia nitrogen at 0.04 ± 0.01 mg/L, and were measured twice a day by a multi-parameter YSI professional-plus probe (Yellow Spring Instrument Co., Yellow Spring, Ohio, USA). The fish were weighed every two weeks after anesthesia by methane sulfonate (MS-222, 40 mg/L, 2 min), and were fasted one day before weighing.

    At the end of the 6-week feeding experiment, all fish were weighed in each tank before fasting for one day. Three fish per treatment were euthanized by MS-222 (70 mg/L, 6 min) to collect gills, livers, muscles, and blood. Serum was collected from the blood, which was clotting for 5 h at 4 ℃ and then centrifuged at 3500 × g for 5 min (Moghaddam et al. 2013). The tissues were then snap-frozen in liquid nitrogen, and were kept at − 80 ℃ until analysis.

    Subsequently, salinity acclimation was carried out. All tanks were rapidly changed in salinity from zero to 15 g/L by adding seawater. Then, the fish were gradually acclimated at a rate of 3 gL−1d−1 until 30 g/L was reached. After that, fish were kept in the tanks for 14 days. The muscles, gills, serum, and livers were collected on days 1, 4, 7, and 14 after seawater acclimation using the methods described above.

    All protocols for animal work were approved by Ocean University of China (Qingdao, China). The approval number is OUC20170516.

  • Measurements and analytical methods

  • The crude protein content of the experimental diets was measured by a Vario ELIII Elemental Analyzer (Elementar, Germany). Crude lipids were determined after the extraction of diethyl ether by the Soxhlet method (Buchi 36, 680, Switzerland). Ash was determined after combustion for 8 h at 550 ℃ in a muffle furnace.

    Serum osmolality was measured with a Fiske 210 micro-osmometer. Serum concentrations of Na+, K+, Ca2+, Mg2+, Cl, gill NKA activity, liver SOD activity, liver CAT activity, and muscle MDA content were tested by commercial kits (Nanjing Jiancheng Bioengineering Institute, Nanjing, China). The concentration of serum cortisol was determined by an ELISA Kit (Shanghai ELISA Biotech Co., Ltd., Shanghai, China). The specific steps were carried out strictly following the manufacturer's instructions. In addition, serum biochemical parameters, including TP, ALB, LDH, ALP, ALT, AST, GLUC, TRIGL, and CHO were determined by an automatic serum biochemical analyzer (Cobas C-311, Roche Diagnostics, Shanghai, China). Serum-free amino acids were determined using automatic amino acid analyzer (L-8900, Hitachi, Japan) following Xu et al. (2016).

  • Statistical analysis

  • All statistical analyses were carried out by SAS 9.4 (SAS Institute Inc., Cary, North Carolina, USA). Data were tested for the normality and homogeneity of variances by Levene's test. Then, data were analyzed by a one-way analysis of variance (ANOVA) followed by the SNK multiple comparisons test to distinguish significant differences between treatment means. Interactions between dietary taurine levels and time on different parameters were evaluated by two-way ANOVA (SNK) among the treatment means. Additionally, comparisons of the serum taurine content were performed and significant differences were evaluated using t-test. All statistical tests were considered significant at P < 0.05. All figures were processed using GraphPad Prism 7 (GraphPad Software, San Diego, CA, www.graphpad.com).

    The fish growth performance parameters were calculated using the following equations:

    FCR = (dry feed offered / wet weight gain)

    Percent weight gain (%) = 100 × (final body weight—initial body weight)/ (initial body weight). The growth rates were calculated as the TGC (Cho 1992).

    where IBW is the initial body weight (g/fish), FBW is the final body weight (g/fish), D is the number of days, and T is the average daily water temperature.

Acknowledgements
  • The authors of this study would like to thank everyone who critically reviewed this manuscript and helped with the sample collection. This study was supported by the National Key Research and Development Program of China (2019YFD0901000), the National Natural Science Foundation of China (31702364 and U1906206), and the OUC-AUBURN Joint Research Center for Aquaculture and Environmental Sciences.

Author contributions
  • YZ and SD guided the experiments. MH, XY, and JG carried out the experiments and analyzed samples. MH analyzed the data and drafted the manuscript. QG, AD, and YD helped edit this manuscript.

Data availability
  • The data that support the findings of this study are available in Supplementary materials.

Compliance with ethical standards

    Conflicts of interest

  • The authors declare that there is no conflict of interest.

  • Animal and human rights statement

  • This study was conducted in accordance with the Institutional Animal Care and Use Committee of the Ocean University of China. All protocols of animal work were approved by the Ocean University of China (Qingdao, China). The approval number is OUC20170516. This study does not contain any studies with human participants.

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