Dimethyl-β-propiothetine (DMPT) supplementation under the all-plant protein diet enhances growth performance, digestive capacity and intestinal structural integrity for on-growing grass carp (Ctenopharyngodon idella)
Introduction
Recently, plant protein sources have been extensively used to replace fishmeal in aquafeeds, due to stagnant fish meal supply and exorbitant price (Anderson et al., 2016). However, studies have reported that the all-plant protein diet lead to some unsatisfactory results such as low FI and poor growth in red sea bream (Pagrus major) (Biswas et al., 2019) and low digestive capability in blunt snout bream (Megalobrama amblycephala) (Abasubong et al., 2019). These adverse effects were ascribed to poor palatability, high antinutritional factors, essential amino acid deficiencies and so on in the diet (Francis et al., 2001; Gatlin Iii et al., 2007). Among these factors, poor palatability is an important factor (Freitas et al., 2011). Studies showed that feeding stimulants are widely used to solve the diet palatability issue and enhance the animal appetite and growth in the all-plant protein diet, such as krill meal in Nile tilapia (Oreochromis niloticus) (Gaber, 2010), and taurine in zebrafish (Danio rerio) (Guimarães et al., 2018). Thus, it is of great necessity to use feeding stimulant to increase FI and improve animal growth performance in an all-plant protein diet.
At present, dimethyl-β-propiothetine (DMPT) is highly commended among feeding stimulants. Previous studies have reported that DMPT improved FI and promoted growth of gold fish (Carassius auratus) (Nakajima, 1996), as well as enhanced digestive ability by improving protease, lipase and amylase activities in the intestine of Gibel carp (Carassius auratus gibelio) (Xue et al., 2007). Nevertheless, a previous report demonstrated that DMPT could react with the hydroxyl radical (·OH) and decrease the free radical content in marine algae (Sunda et al., 2002). Another study indicated that the decreased free radical content could reduce oxidative damage in gerbils (Lu et al., 2012). Moreover, digestive function has been found to depend in part on the intestinal structural integrity, which could be influenced by oxidative damage to some extent (Chiva et al., 2003; Shoji et al., 2007; Wei et al., 2018). According to the above studies, DMPT, apart from enhancing animals' FI, we speculate that it might relieve oxidative damage to the intestines of fish. However, there is hardly any report regarding DMPT on this intriguing topic, which is worthy of investigation.
To our knowledge, oxidative damage can be relieved by antioxidant systems which benefit in scavenging excess levels of free radicals in fish (Martínez-Álvarez et al., 2005). Fish antioxidant systems are composed of non-enzymatic compounds and antioxidant enzymes (Jiang et al., 2018). Different antioxidant enzyme genes play different roles or functions in regulating antioxidant ability in animals (Jiang et al., 2017). Glutathione peroxidase type 1(GPx1) is responsible for protecting cells from damage caused by hydrogen peroxide, whereas GPx4 mainly inhibits the membrane phospholipid peroxidation (Chen et al., 2012; Ran et al., 2004). Glutathione S-transferase omega (GSTO) conjugates the several products of oxidative stress, glutathione S-transferase P (GSTP) detoxifies a range of compounds such as DNA and RNA hydroperoxides, and glutathione S-transferase R (GSTR) is responsible for conjugating 4-hydroxynonenal produced by lipid peroxidation (Espinoza et al., 2013). Copper zinc superoxide dismutase (CuZnSOD) and manganese superoxide dismutase (MnSOD) are located in the cytoplasm and the matrix of mitochondria in fish, respectively (Umasuthan et al., 2012). Furthermore, it was reported that antioxidant enzyme genes expression could be regulated by NF-E2-related factor 2 (Nrf2) signalling pathway in fish (Yao et al., 2007). However, until now, studies concerning the effect of DMPT on oxidative damage, antioxidant ability and the related signalling pathways in animal intestine are scarce. A previous study has indicated that DMPT provided a methyl donor and participated in methionine synthesis in rats (Dubnoff and Borsook, 1948). Our laboratory study showed that methionine enhanced non-enzymatic compound glutathione (GSH) content and activities of antioxidant enzymes including superoxide dismutase (SOD) and catalase (CAT) in the intestines of grass carp (Ctenopharyngodon idella) (Wu et al., 2017). Wang et al. (2014) reported that DMPT improved the muscle protein level of taimen (Hucho taimen). In human, the improved protein level was shown to increase glucagon-like peptide 1 (GLP-1) release (Geraedts et al., 2010), which could activate the Nrf2 signalling in endothelial cells (Pujadas et al., 2015). Thus, these results indicated a possible relationship between DMPT and fish intestinal oxidative damage, antioxidant ability and the related Nrf2 signalling pathway, which is worthy of further investigation.
Grass carp is an herbivorous fish with the largest production in global freshwater aquaculture (He et al., 2017), and the fish meal proportion in the current commercial formulation of this species was approximately 3.0–5.0% (Chen and Zhang, 2019; Wu et al., 2018). At present, the appropriate DMPT supplementation level for grass carp has only been investigated in the juvenile stage of grass carp under low fish meal diet (Zhang et al., 2011). However, the appropriate supplementation levels of feeding stimulants may vary with content of fish meal in diets and different growth stages, such as taurine in rainbow trout (Oncorhynchus mykiss) (Gaylord et al., 2010) and turbot (Scophtalmus maximus) (Qi et al., 2012). Until now, there has been no study investigating the appropriate levels of DMPT supplementation for on-growing grass carp under the all-plant protein diet, which requires investigation.
Taken together, this study is the first to evaluate the appropriate level of DMPT supplementation under the all-plant protein diet for the on-growing grass carp, which may provide a reference for the commercial non-fish meal diet formulation and healthy breeding of this fish. Meanwhile, using grass carp as a research model, apart from investigating the effects of dietary DMPT supplementation on growth performance and digestive capacity, we investigated the relationship between DMPT and oxidative damage and antioxidant ability as well as the related Nrf2 signalling, which could provide a partial theoretical basis and molecular mechanisms for DMPT regulating the structural integrity in the intestines of fish and animals, for the first time. This study also provided new ideas for the study of feeding stimulant.
Section snippets
Experimental diet preparation
The composition of the fish meal (FM) diet and the all-plant protein diet (FM entirely replaced by soybean-condensed protein) are presented in Table 1. The FM diet and the all-plant protein diet were formulated to be isonitrogenous and isolipidic. The FM diet was used to compare the diet efficacy with the DMPT supplementation diet group according to the method from a previous study (López et al., 2015). In the all-plant protein diet, soybean-condensed protein (SPC) replaced all fish meal of the
The effects of DMPT supplementation under the all-plant protein diet on growth performance, intestinal growth and neuropeptide Y (NPY) content in the brain of on-growing grass carp
As shown in Table 3, there were no noticeable differences on the IBW and ISI among all the treatments groups (P > .05). Compared with the fish meal (FM) diet group, the all-plant protein diet group (un-supplemented DMPT) significantly lowered the FBW, PWG, SGR, FI, IL, ILI, IW and NPY content in the brains of on-growing grass carp (P < .05). However, compared to the all-plant protein diet group, dietary DMPT supplementation significantly increased these parameters of on-growing grass carp (P
The all-plant protein diet reduced growth performance, decreased digestive ability and impaired intestinal structural integrity of on-growing grass carp
As a result of the shortage and high price of fish meal, the use of plant protein in aquafeed is of great significance in maintaining the sustainable development of aquaculture industry (Zhang et al., 2018). In this study, we explored the effect of the all-plant protein diet on on-growing grass carp. The current study showed that compared with the FM diet group, the all-plant protein diet group (un-supplemented DMPT) reduced FI and PWG, lowered intestinal growth (IL and IW) and digestive
Conclusions
In summary (Fig. 5), the present study confirmed that the all-plant protein diet compromised fish FI, growth and digestive capacity, and DMPT supplementation under the all-plant protein diet effectively reversed the adverseness. Based on the quadratic regression analysis for optimal growth performance indices (FI and PWG) and oxidative damage indices (PC and MDA) of on-growing grass carp under the all-plant protein diet, the appropriate levels of DMPT supplementation were estimated as to be
Acknowledgements
This research was financially supported by National Key R&D Program of China (2018YFD0900400), the Earmarked Fund for China Agriculture Research System (CARS-45), Key Research and Development Plan in Sichuan Province (2018NZ0007), Outstanding Talents and Innovative Team of Agricultural Scientific Research (Ministry of Agriculture), Foundation of Sichuan Youth Science and Technology Innovation Research Team (2017TD0002), Supported by Sichuan Science and Technology Program (2019YFN0036). The
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2022, AquacultureCitation Excerpt :However, there are still major challenges in fishmeal substitution, which had negative effects on the growth performance (Anderson et al., 2016; Liu et al., 2019), fillet texture and nutritive values of aquatic species fed diets with high-level plant feed stuffs (Hu et al., 2018; Wu et al., 2021). It is speculated that this performance is due to the presence of anti-nutritional factors (ANFs), unbalanced amino acids profiles and/or poor palatability, and other differences between plant protein sources and fish meal could also be important (Anderson et al., 2016; He et al., 2019; Li et al., 2020a; Liu et al., 2019; Michelato et al., 2016). As an essential amino acid (EAA) for aquatic animals, methionine (Met) is the main limiting amino acid, but Met was poor in plant-source feedstuffs (He et al., 2019).
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