Abstract
As an important protein source, soybean products can cause intestinal inflammation and injury in many animals including human beings, particularly infants and juvenile individuals. Research in this field has been performed for terrestrial animals and fish, but still lacks integrity and systematicness. In this study, the main biological processes in the intestinal tract of marine fish juvenile pearl gentian grouper in the state of soybean meal-induced enteritis (SBMIE) were analyzed. A total of 720 groupers with an approximate initial weight of 12.5 g were randomly divided into three groups: the fish meal (FM) control group, the 20% SBM group (SBM20), and the SBM40 group (n = 4). Three iso-nitrogenous and iso-lipidic diets were prepared and fed to fish for 10 weeks. Each barrel contained a water volume of about 1 m3 in and was exposed to natural light and temperature. Results indicated that the growth and physiology of groupers fed with SBM were significantly negatively affected, with the gene expressions of intestinal structural protein abnormal. 16SrDNA high-throughput sequencing showed that the intestinal microflora played an important role in the pathogenesis of pearl gentian grouper SBMIE, which may activate a variety of pathogen pattern recognition receptors, such as toll-like receptors (TLRs), RIG-I-like receptors, and nod-like receptors. Transcriptome analysis revealed that changes of the SBMIE signaling pathway in pearl gentian groupers were conservative to some extent than that of terrestrial animals and freshwater fish. Moreover, the TLRs-nuclear factor kappa-B signaling pathway becomes activated, which played an important role in SBMIE. Meanwhile, the signal pathways related to nutrient absorption and metabolism were generally inhibited. Metabolomics analysis showed that isoflavones and saponins accounted for a large proportion in the potential biomarkers of pearl gentian grouper SBMIE, and most of the biomarkers had significantly positive or negative correlations with each other; 56 metabolites were exchanged between intestinal tissues and contents, which may play an important role in the development of enteritis, including unsaturated fatty acids, organic acids, amino acids, vitamins, small peptides, and nucleotides, etc. These results provide a basic theoretical reference for solving the intestinal issues of fish SBMIE and research of inflammatory bowel disease in mammals.
Highlights
Since the beginning of 1990, fishery production has stagnated at about 90 million tons, and aquaculture is expected to meet the global demand for marine food in the future[1]
The transmission electron microscopy (TEM) data shows that the goblet-cell number gradually increases with the increase of soybean meal (SBM) substitute level (Fig. 2A,C,E), and the intercellular junctions in experimental groups become progressively worse in comparison to the fish meal (FM) group (Fig. 2B,D,F)
The present study shows that the growth performance, intestinal morphology, intestinal microflora composition and abundance, and immune-related gene expressions of pearl gentian grouper were clearly affected by the SBM substitute for FM
Summary
Since the beginning of 1990, fishery production has stagnated at about 90 million tons, and aquaculture is expected to meet the global demand for marine food in the future[1]. Common SBMs can only be added to feed at a low level, otherwise, it may affect the intestinal microflora structure and cause enteritis in the hindgut of fish, such as Salmo salar[4], Oncorhynchus mykiss[5], Cyprinus carpio[6], and Danio rerio[7], etc. SBM may increase the harmful microflora abundance in the intestines of Salmo salar[11], Oncorhynchus mykiss[12], and Gadus morhua[13], and cause inflammation. The exact reasons for SBMIE and other negative effects are not fully understood, but related studies have indicated alcohol-soluble ANFs, especially soybean saponins, to be the main potential pathogenic factor[14]. The results suggested that the interaction between different ANFs is very important, but the mechanism of the effects of different ANFs on intestinal health is not fully understood
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