Effects of bio-fermented feed on growth, digestion, immunity, antioxidant capacity, and intestinal structure of juvenile yellow catfish (Pelteobagrus fulvidraco)

doi:10.21203/rs.3.rs-3238909/v1

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Effects of bio-fermented feed on growth, digestion, immunity, antioxidant capacity, and intestinal structure of juvenile yellow catfish (Pelteobagrus fulvidraco)

https://doi.org/10.21203/rs.3.rs-3238909/v1

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To investigate the feeding effect of fermented feed, juvenile yellow catfish (1.23±0.54) g were fed with hard pellet feed and biological fermented feed in an indoor recirculating water system for 8 weeks. The study analyzed the effects of fermented diets on the growth performance, digestion, immunity, antioxidant capacity, and intestinal structure of yellow catfish. The results showed that: the fermented diet significantly increasedthe WGR, SGR, and VSI, but had no significant effect on the HSI. The fermented diet significantly increased the activities of Try, Lip, and AMS in the intestinal tract of yellow catfish. The fermented diet significantly increased the activities of ACP, AKP, CAT, and SOD in the serum of yellow catfish and significantly decreased the content of MDA in the serum. The fermented diet significantly increased the width and height of the intestinal villus and the thickness of the intestinal wall in the midgut of yellow catfish.The results indicate that fermented feed could effectively improve the growth performance, digestive enzyme activity, and immune and antioxidant capacity, and improve the intestinal tissue structure of yellow catfish. This provides a theoretical basis for the production of microbial fermented feed.

yellow catfish

fermented feed

immunization

antioxidant capacity

structure of the intestine

Fermentation technology has been utilized in food processing and preservation for centuries ^[1]. Through artificial control of fermentation temperature, water, and other conditions, fermented feed, rich in beneficial microorganisms and decomposition products through the metabolism of specific strains based on feed raw materials or compound feeds, is produced ^[2]. Raw materials commonly used in the production of biologically fermented feed include straw, cassava residue, bacterial bran, cotton tea cake, lower fruit residue, and distiller's grains ^[3]. Fermentation significantly increases nutrients such as crude protein, soluble protein, and polyunsaturated fatty acid, and some fermentation components can also act as immune enhancers ^[4]. The improvement in nutrients like soluble protein ^[5–7] can help enhance the growth performance and digestibility of aquatic animals. The metabolites of probiotics during fermentation ^[8–10] can improve the immunity and antioxidant capacity of aquatic animals, and the metabolic activities of probiotics during fermentation ^[11–13] can improve the intestinal structure of aquatic animals. Multiple studies on aquatic animals such as Largemouth bass ^[14], Zebrafish ^[15], and African catfish ^[16] have determined that fermented diets produced through the fermentation process result in improved growth performance, digestibility, immunity, and change in the intestinal structure of aquatic animals.

The yellow catfish (Pelteobagrus fulvidraco) is an omnivorous freshwater fish that is widely distributed in the inland areas of our country. In recent years, it has been widely welcomed in the market because of its tender flesh and high nutritional value^[17]. With the improvement of artificial breeding technology and pond intensification, the yield per mu of yellow catfish has been greatly improved^[18]. Abnormal nutritional metabolism and breeding environment problems accompanied by high-density cultivation will lead to the decline of growth rate and frequent diseases of yellow catfish, resulting in serious economic losses to farmers and restricting the healthy and sustainable development of yellow catfish aquaculture^[19]. The application of nutritional immunology to improve the immunity of farmed animals has been widely recognized and is considered an important technical means to produce high-quality farmed animals^[20]. Because of the lack of theoretical research and practical application of bio-fermented feed on Pelteobagrus fulvidraco, this study took Pelteobagrus fulvidraco as a research object and measured its growth performance, digestive enzyme activity, immunity, antioxidant capacity, and intestinal structure, to provide a reference for the application and promotion of bio-fermented feed in the breeding and production of Pelteobagrus fulvidraco.

Experimental diet

The bio-fermented feed (Fermentation group) and hard pellet feed (Control group) used in the experiment were provided by Jingzhou Zhanxiang Feed Co., LTD. The hard pellet feed was made from fish meal, soybean meal, flour, and other raw materials. The biologically fermented feed was produced through the catabolism of plant Lactobacillus and Saccharomyces cerevisiae, using appropriate processing techniques. The nutrient contents of the experimental diets are presented in Table 1.

Table 1

Nutrient content of experimental diets (dry matter basis)
	Control group	Fermentation group
Crude protein	44.19^a	45.82^a
Crude fat	10.82^a	10.14^a
Ash	10.92^a	12.76^a

Values represent means ± SD. Different letters in the same row indicate a significant difference between groups (P < 0 .05).

Experimental procedures

The initial body weight of the juvenile yellow catfish used in the experiment was (1.23 ± 0.54 g) and they were purchased from the Jingmen Shayang County breeding base. They were temporarily kept in the indoor recirculating water system of rooms 5-410 in Yangtze University's West Campus in Jingzhou, Hubei Province. Before being temporarily kept, the breeding box was disinfected using potassium permanganate. Uniform specimens were selected without any disease symptoms for the experiment.

The experiment involved the use of an indoor recirculating water system, where a control group and a fermentation group were established. Six tanks with a volume of 40 liters each were randomly selected, and 20 juvenile yellow catfish were placed in each tank, with 3 replicates in each group. The experiment lasted for 56 days. The fish were fed twice a day (at 9:00 and 17:00) with the daily feeding amount being 3%-5% of the body weight. The feeding amount was recorded. Throughout the experiment, the water pH was maintained at 7.0 ± 0.5, the dissolved oxygen level was not less than 0.1 mg/L, and the ammonia nitrogen content was kept below 0.1 mg/L.

Sample Collection

After the culture experiment was completed, juvenile yellow catfish were fasted for 24 hours. The fish were then removed and the water on their surface was wiped dry. The body weight, body length, and total length of the fish were accurately measured, and the survival rate in each tank was counted. After weighing, 18 fish were randomly selected from each tank, and blood was collected from their tail veins using a 1 mL disposable syringe without heparin infiltration. The collected blood was left to stand overnight at 4 ℃, and then centrifuged at 4000 g/min at 4 ℃ for 10 minutes. The resulting supernatant was stored at -80 ℃ for later use. The fish were then rapidly dissected, and the liver was removed and weighed. One juvenile yellow catfish from each tank was randomly selected to have its midgut removed and placed in tissue-fixative solution. These specimens were sent to Wuhan Sevier Biotechnology Co, LTD for the preparation of intestinal sections. The remaining juvenile yellow catfish midgut, placed in sterile EP tubes, was stored at -80 ℃ for digestive enzyme determination. Three whole fish were randomly selected from each tank and stored at -80 ℃ for body composition determination.

Analytical methods

The formula for measuring growth performance is as follows:

Weight gain rate (WGR,%) = (W_f-W_i) /W_i×100;

Specific growth rate (SGR,%) =(InW_f-InW_i)/d×100;

Survival rate (SR,%) = (N_f/N_i) ×100;

Hepatopancreas somatic indices (HSI,%) = W_h/W×100;

Coefficient of fullness (CF,g/cm³) = W/L³×100;

Organ/body weight ratio (VSI) = (W_v/W_i) ×100%.

Note

W_f= fish weight at the end of the test; W_i=fish body weight before the test; N_f= number of fish tails surviving at the end of the test; N_i= initial mantissa of fish before the test; W_h= liver weight; W = fish weight; L = body length; d breeding days; W_v= fish viscera mass at the end of the test.

Analysis of essential nutrients

The water content of the diet was determined by drying at 105°C under normal pressure (GB/T 6435 − 1986). Crude protein content was determined by the Kjeldahl method (GB/T 6433 − 2006). Crude fat content was determined by the light petroleum extraction method (GB/T 6433 − 2006). Crude ash content was determined by cauterization method at 550°C (GB/T 6438 − 1992).

Intestinal tissue sections

The intestinal tissue was removed from the fixative, dehydrated with an ethanol gradient, embedded in paraffin, cut into 7 µm sections using a tissue microtome, stained with hematoxylin and eosin (HE), and sealed with neutral gum. Images were taken with a light microscope, and the height of the plica and the thickness of the muscle layer were measured using Image-Pro Plus 6 software.

Digestive enzyme activity

To determine the intestinal digestive enzyme activity, fresh intestinal tracts (approximately 0.1 g) were accurately weighed and placed in a 10 ml homogenate tube. Nine times the volume of deionized water was added, homogenized in an ice bath using a homogenator, and centrifuged (3000 g.min, 10 min, 4°C). The supernatant was collected, and protein quantification was determined by the Coomassie brilliant blue method. The alpha-amylase activity was measured by starch-iodine colorimetry, trypsin activity was measured by UV colorimetry, and lipase activity was measured by a triglyceride colorimetric assay. All kits used were purchased from Nanjing Jiancheng Biotechnology Co., LTD.

Immune and antioxidant indexes

The activities of acid phosphatase and alkaline phosphatase were measured using the phenyl-disodium phosphate method with 1 mg phenol produced by 100 ml serum at 37 ℃ for 15 minutes defined as one unit of activity. Catalase activity was measured using the ammonium

molybdate method with the amount of 1 µmol of hydrogen peroxide decomposed per milliliter of tissue protein per second defined as one unit of activity. The xanthine oxidase method was used to measure superoxide dismutase (SOD) activity with the amount of SOD corresponding to 50% inhibition of SOD in 1 ml reaction solution per ml tissue protein defined as one unit of activity. The content of malondialdehyde was determined using the thiobarbituric acid method. All kits utilized were purchased from Nanjing Jiancheng Biotechnology Co.

Data statistics and analysis

All results were expressed as mean ± standard deviation (SD) and the results were statistically analyzed using Excel and SPSS software. One-way ANOVA was used to compare data between the fermented diet group and the control group, and Duncan's test was used for multiple comparisons, with P < 0.05 considered a significant difference.

Effects of bio-fermented diets on the growth performance of yellow catfish

The growth performance of juvenile yellow catfish is shown in Table 2. The weight gain rate, specific growth rate, and final body weight of the fermentation group were significantly higher than those of the control group ( P < 0.05). The coefficient of fullness and organ/body weight of the fermentation group were higher than those of the control group, but the differences were not significant ( P > 0.05).

Table 2

Effects of different diets on growth performance of *Yellow catfish* (Pelteobagrus fulvidraco)
Indexes	Control group	Fermentation group
Original weight/g	1.82 ± 0.54	1.82 ± 0.54
Terminal weight/g	9.51 ± 2.06^a	13.22 ± 2.11^b
Weight gain rate/%	422.71 ± 22.89^a	626.34 ± 26.52^b
Specific growth rate/(%/d)	2.95 ± 0.08^a	3.54 ± 0.06^b
Coefficient of fullness/(g/cm³)	1.33 ± 0.02	1.39 ± 0.03
Organ/body weight ratio/%	1.23 ± 0.14	1.13 ± 0.10
Liver body ratio/%	5.66 ± 1.38	5.71 ± 0.63
Survival rate/%	97.83 ± 2.89	97.63 ± 2.89

Values represent means ± SD. Different letters in the same row indicate a significant difference between groups (P < 0 .05).

Effects of bio-fermented feed on digestive enzyme activities of yellow catfish

After 8 weeks of feeding trial, the digestive enzyme activities in the intestinal were shown in Fig. 1 (A, B, and C). The AMS, Try, and Lip in the midgut of the fermentation group were significantly higher than those of the control group ( P < 0.05).

Immune and antioxidant properties of yellow catfish fed a bio-fermented diet

The immune and antioxidant properties of juvenile yellow catfish are shown in Fig. 2. The activities of AKP, ACP, CAT, and SOD in the serum of the fermentation group were significantly higher than those of the control group (P < 0.05; Fig. 2A, B, C and E). The MDA content in the serum of Pelteobagrus fulvidraco in the fermentation group was significantly lower than that in the control (P < 0.05; Fig. 2D).

Effects of biofermented diets on intestinal tissue structure of juvenile yellow catfish

As shown in Fig. 3, the intestinal wall thickness, villus height, and width of the control group were 97 ± 4.899, 401.25 ± 9.7109, and 85.5 ± 10.786, respectively. Compared with the control, the intestinal wall thickness, villus height, and villus width of the fermented food group increased significantly by 36.59%, 37.32%, and 34.56%, respectively (P < 0.05).

Effects of bio-fermented diets on the growth of yellow catfish

In this experiment, feeding Pelteobagrus fulvidraco with bio-fermented feed significantly increased WGR, SGR, and VSI of juvenile Pelteobagrus fulvidraco. These results indicated that the bio-fermented diet can significantly enhance the growth and development of juvenile yellow catfish. Relevant studies have shown that the final body weight, WGR, and SGR of Procambarus clarkii are significantly increased after feeding Procambarus clarkii with 30% kitchen waste fermentation ^[21]. The study on Largemouth bass also showed that biologically fermented diets significantly increased the WGR and SGR of Largemouth bass^[22]. The study on injury in Litopenaeus vannamei showed that biologically fermented feed could improve the survival rate and body weight of Litopenaeus vannamei^[23]. Studies on Nile tilapia have shown that adding 5% Lactobacillus fermented soybean meal or 5% Saccharomyces cerevisiae fermented soybean meal to the diet can significantly increase the weight gain rate and specific growth rate of Nile tilapia^[24]. Biological fermentation technology can reduce the anti-nutritional factors in feed raw materials and release active substances. In addition, fermentation breaks down macromolecules into small peptides, amino acids, and other easily absorbed substances. After fermentation, nutrients such as crude protein, soluble protein, and polyunsaturated fatty acids are significantly increased ^[25–26], making it easier for the body to absorb and utilize these nutrients, so that fermented diets can improve the growth performance of the animal body.

Effects of bio-fermented diets on intestinal digestive enzyme activities of yellow catfish

In this study, feeding the bio-fermented feed significantly increased the activities of AMS, Try, and Lip in juvenile yellow catfish. Therefore, the bio-fermented feed can improve the intestinal enzyme activities of Pelteobagrus fulvidraco to a certain extent. The study showed that the protease and amylase of Litopenaeus vannamei were significantly higher than those of the control group after 21 days of feeding, and those of the control group after 42 days of feeding^[27]. In the experiment of using fermented soybean meal instead of fish meal in the diet of Seriola lalandi, Nguyen found that the addition of taurine to the fermented soybean meal resulted in the lipase activity of Seriola quinqueradiata and the control phase ^[28]. In the experiment of using four fermented soybean meals instead of fish meal in the diet of turbot, Dan found that the amylase activity of turbot in the 33% Bacillus fermented soybean meal instead of fish meal group and the 32% yeast fermented soybean meal instead of fish meal group was higher than that of the fish meal group, but the difference was not significant. The trypsin activity of Scophthalmus maximus flounder in the 33% Bacillus fermented soybean meal instead of fish meal group was significantly higher than that in the fish meal group^[29]. The growth index of fish is closely related to the digestive and absorptive capacity of the fish intestine, and intestinal digestive enzymes and brush border membrane enzymes play an important role in the process of digestion and absorption of nutrients ^[30]. After the feed is fermented, its attractiveness and palatability can be improved to promote animal feeding. In addition, during the fermentation process of feed, some macromolecular substances such as proteins are broken down into small molecules through a series of biochemical reactions, which are easier for animals to absorb ^[31].

Effects of a bio-fermented diet on immunity and antioxidant capacity in juvenile yellow catfish

Oxidative stress in fish cells is caused by excess reactive oxygen species, such as superoxide anions and hydroxyl radicals, which predispose the organism to age and disease ^[32]. SOD is an important functional enzyme in the antioxidant defense system of organisms, which can remove reactive oxygen free radicals in the body and reduce lipid peroxidation damage. Increasing SOD activity can be seen as an adaptive metabolic response of organisms to reduce lipid peroxidation damage ^[33]. As the end product of lipid oxidation in animals, MDA levels may indirectly reflect the degree of oxidative damage in fish, and the higher the level, the more severe the damage ^[34]. AKP and ACP are important detoxification enzymes that regulate the body's phosphorus metabolism and carry out non-specific immunity to environmental toxic stress ^[29]. In this study, the bio-fermented feed should significantly increase the serum levels of SOD, CAT, ACP, and AKP and significantly decrease the content of MDA in juvenile yellow catfish compared with the control. Related studies have shown that replacing soybean meal with fermented soybean residues in the diet of largemouth bass can significantly increase the activities of SOD and CAT and decrease the level of MDA in the serum of Largemouth bass^[33]. CAT activity in grass carp can be improved by adding fermented leaves to the grass carp diet[35]. Dossou et al. found in the experiment of adding 285g/kg of fermented rapeseed meal to the diet of Red snapper that the serum MDA concentration of red sea bream in the fermented rapeseed meal group was significantly lower than that of the control group ^[36]. Chen's study found that fermented wheat bran could upregulate the mRNA expression of CAT ^[34], which may be the reason why the activity of CAT was increased. Probiotic bacteria present in fermented feed can effectively colonize the intestinal tract of yellow catfish, leading to improvements in the composition of the microbial community. Furthermore, these probiotics facilitate the production of beneficial prebiotics, particularly during their growth and reproduction stages. The symbiotic interaction between probiotics and prebiotics is believed to be the underlying mechanism through which fermented feed reinforces the immune system and enhances the antioxidant capacity of yellow catfish.

Effects of bio-fermented feed on intestinal tissue structure in yellow catfish

The intestinal tract is an important digestive organ and the largest micro-ecosystem in the body. At the same time, it has functions such as immunity and detoxification, which maintain the good digestion and absorption function of the intestinal tract of fish and play an important role in the rapid growth and disease resistance of fish ^[37]. The height, width, number, and morphological structure of intestinal villi reflect the strength of intestinal digestion and absorption capacity to a certain extent ^[38]. The muscle layer is related to the rhythmic intestinal peristalsis of aquatic animals, and the integrity of the muscle layer can reflect the mechanical digestive capacity of the intestine ^[39–41]. In this experiment, compared with the hard pellet diet, the biological fermented diet can increase the thickness of the midgut muscle layer, and the height, and width of the intestinal villi of yellow catfish. Wang found that using fermented soybean meal instead of fish meal in the diet of Pseudosciaena crocea could significantly increase the number of goblet cells in the intestine of Pseudosciaena crocea^[37]. Yang in the experiment of using fermented soybean meal instead of fish meal in the diet of Largemouth bass found that the intestinal villus height, muscle layer thickness, and intestinal villus circumference of Largemouth bass in the group replacing 100 g/kg fish meal with 224.7 g/kg fermented soybean meal and replacing 150g/kg fish meal with 299.6g/kg fermented soybean meal were significantly higher than those in the fish meal group ^[38]. Ismail et al. added 5–20% fermented olive meal to the diet of Nile tilapia and found that the number of intestinal goblet cells of Nile tilapia gradually increased with increasing levels of olive meal ^[42]. The inclusion of fermented feed led to a substantial augmentation in both the height and width of intestinal villi in yellow catfish, clearly indicating an expansion in the surface area of the intestine and an enhanced capacity for efficient nutrient absorption and digestion. Furthermore, the observed thickening of the muscular layer suggests a bolstered mechanical digestion capability, which provides a plausible explanation for the higher levels of digestive enzyme activity observed in the yellow catfish fry fed with fermented feed. The enhancement of intestinal structure in Pelteobagrus fulvidraco through the use of fermented feed can be attributed to the incorporation of beneficial microorganisms like lactic acid bacteria and yeast in the fermentation process. These advantageous bacteria have the potential to bolster the population of beneficial microbes within the intestines. By competing with harmful bacteria for resources and attachment sites, they effectively restrict the growth of detrimental bacteria. Moreover, these beneficial microorganisms generate beneficial metabolites like organic acids and antimicrobial substances, thus significantly improving the intestinal environment^[43].

Feeding after fermentation treatment can effectively improve the growth performance, digestive enzyme activity, immune enzyme activity, and antioxidant capacity of yellow catfish, and can improve the intestinal structure of yellow catfish, promote the growth of other probiotics, and better play its probiotic role.

Author contribution Zexiang Zhou;Xueru Zhao;Jiu Shu: investigation, data curation, and writing-original draft. Liu Fang: conceptualization, methodology, and writing-review and editing. Qian Wang: software, validation, visualization, and project administration. Guoliang Ruan: methodology, investigation, and writing-review and editing.All authors read and approved the fnal manuscript.

Funding

Data availability The data that support the fndings of this study are available from the corresponding author, Liu Fang, upon reasonable request.

Conclusions

Competing interests The authors declare no competing interests

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Competing interest reported. Declaration of Interest: The authors hereby declare that there are no significant or potential conflicts of interest in relation to the writing of this paper. We affirm that during the preparation of this paper, we have received no grants, financial support, or any other form of sponsorship that could result in a conflict of interest or influence our perspectives or conclusions. Our research and writing are conducted independently, relying solely on objective data and our own analysis. Furthermore, we confirm that we have no direct or indirect affiliations with any commercial organizations or other stakeholder groups. Our research is driven by academic curiosity and the desire to advance scientific knowledge, unaffected by any external interests or pressures. We firmly believe that transparent disclosure of potential conflicts of interest is crucial to ensuring the quality and academic integrity of research papers. We encourage other authors and researchers to likewise adhere to this principle, providing accurate and transparent declarations of interest in their own work. Please be assured that our study, as well as the findings and conclusions presented in this paper, are based on objective analysis and authentic data, with the aim of fostering academic progress and knowledge dissemination. Thank you for your attention and cooperation. Sincerely, Liu Fang

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Effects of bio-fermented feed on growth, digestion, immunity, antioxidant capacity, and intestinal structure of juvenile yellow catfish (Pelteobagrus fulvidraco)

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Introduction

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Experimental diet

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Immune and antioxidant indexes

Data statistics and analysis

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