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Multiomics analysis of soybean meal induced marine fish enteritis in juvenile pearl gentian grouper, Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂.

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.

SUBMITTER: Zhang W

PROVIDER: S-EPMC8640039 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Due to diminishing fish meal (FM) supplies, superb protein (PRO) sources are needed for aquaculture, such as soy-based PRO. However, these can cause enteritis and even intestinal injury in fish when used at high proportions in feed. This research examines the effects of substituting soybean protein concentrate (SPC) for FM on the growth performance and intestinal balance of pearl gentian groupers and investigates the mechanism of SPC-induced enteritis. Experimental fish (n = 720) were fed 1 of 3 following diets: (1) a 50% FM diet (control), (2) a diet with 20% of the FM substituted with SPC (group SPC20), and (3) a 40% SPC-substituted diet (SPC40). Fish were fed for 10 wk iso-nitrogenous (50% PRO) and iso-lipidic (10% lipid) diets. Groups SPC20 and SPC40 showed significantly lower developmental performance and intestinal structures than control. Group SPC40 had significantly higher expressions of pro-inflammatory-related genes, such as interleukin 1β (IL1β), IL12, IL17 and tumor necrosis factor α and significantly lower expressions of anti-inflammatory-related genes, such as IL5, IL10 and transforming growth factor β1. Biochemical and 16S high-throughput sequencing showed that the abundance and functions of intestinal flora in group SPC40 were significantly affected (P < 0.05), and there were significant correlations between operational taxonomic unit abundance variations and inflammatory gene expressions at genus level (P < 0.05). The second- and third-generation full-length transcriptome sequence was used to analyze the mechanism of SPC-induced enteritis in pearl gentian groupers, which showed that enteritis induced by SPC may be caused by disturbances to intestinal immune function induced by an imbalance in intestinal nutrition and metabolism, such as the intestinal immunity network for IgA production pathway. However, it remains unclear as to which intestinal immune or nutritional imbalance is most important in enteritis development. This study provides a basis for further research into soy PRO-related enteritis in fish.

Project description:Pattern recognition receptors (PRRs) can recognize microbial-specific pathogen-associated molecular patterns, initiate signal cascade transduction, activate the expressions of host immunity and proinflammatory genes, and, ultimately, trigger an immune response against identified pathogens. The present study focused on two outcomes of feeding pearl gentian groupers with high levels of soybean meal (SBM): (1) growth performance and (2) the intestinal environment, including tissue structure, flora profile, and immune responses. Some 720 groupers were randomly divided into three groups (n = 4): (1) controls, fed a 50% fish meal feed (FM), (2) with 20% of the FM substituted with SBM (SBM20), and (3) 40% of the FM substituted with SBM (SBM40). The fish were fed these iso-nitrogenous and iso-lipidic diets for 10 weeks. They were kept in containers with 1 m3 of water under natural light and temperature levels. The experimental results demonstrate that the SBM diets significantly degraded growth performance and intestinal physiology. Typical enteritis characteristics and immune fluctuations appeared, as reflected by the enzyme activities of total superoxide dismutase and lysozyme, and the contents of immunoglobulin M, complement 3, and complement 4. 16SrDNA high-throughput sequencing showed that the intestinal flora was significantly affected, with the abundance of harmful bacteria, such as Vibrio and Streptococcus, increasing with dietary SBM level. Based on "3 + 2" full-length transcriptome sequencing, three triggered PRRs were found in the intestine: the RIG-like receptor, NOD-like receptor, and Toll-like receptor signaling pathways. The intestinal flora variations were significantly correlated with the activation of the three PRR signaling pathways by canonical correlation analysis. These culminated in the transcriptome activation of NF-κB, IRFs, and costimulatory molecules, ultimately promoting the expressions of proinflammatory cytokines, interferons (IFNs), chemokines, and other molecules vital to the innate and/or adaptive immune responses. This study provides new information for diagnosing and preventing SBMIE in aquaculture fish.

Project description:Iso-nitrogenous and iso-lipidic diets containing 0%, 3%, 6%, 9%, and 12% hydrolyzed porcine mucosa (namely, HPM0, HPM3, HPM6, HPM9, and HPM12) were prepared to evaluate their effects on the growth performance, muscle nutrition composition, texture property, and gene expression related to muscle growth of hybrid groupers (Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂). Groupers were fed to apparent satiation at 08:00 and 16:00 every day for a total of 56 days. It was found that the weight gain percentage in the HPM0, HPM3, and HPM6 groups did not differ (P > 0.05). The cooking loss and drip loss of the dorsal muscle in the HPM3 group were lower than those in the HPM6 and HPM9 groups (P < 0.05). The hardness and chewiness of the dorsal muscle in the HPM3 group were higher than those in the HPM0, HPM9, and HPM12 groups (P < 0.05). The gumminess in the HPM3 group was higher than that in the HPM9 and HPM12 groups (P < 0.05). The total essential amino acid content of the dorsal muscle in the HPM12 group was higher than that in the HPM0 group (P < 0.05). The contents of total n-3 polyunsaturated fatty acid and total n-3 highly unsaturated fatty acid, as well as the ratio of n-3/n-6 polyunsaturated fatty acid in the dorsal muscle was higher in the HPM0 group than in all other groups (P < 0.05). The relative expressions of gene myogenic factor 5, myocyte enhancer factor 2c, myocyte enhancer factor 2a, myosin heavy chain, transforming growth factor-beta 1 (TGF-β1), and follistatin (FST) were the highest in the dorsal muscle of the HPM3 group. The results indicated that the growth performance of hybrid grouper fed a diet with 6% HPM and 27% fish meal was as good as that of the HPM0 group. When fish ingested a diet containing 3% HPM, the expression of genes TGF-β1 and FST involved in muscle growth were upregulated, and then the muscle quality related to hardness and chewiness were improved. An appropriate amount of HPM could be better used in grouper feed.

Project description:Vibrio harveyi causes vibriosis in nearly 70% of grouper (Epinephelus sp.), seriously limiting grouper culture. As well as directly inhibiting pathogens, the gut microbiota plays critical roles in immune homeostasis and provides essential health benefits to its host. However, there is still little information about the variations in the immune response to V. harveyi infection and the gut microbiota of grouper. To understand the virulence mechanism of V. harveyi in the pearl gentian grouper, we investigated the variations in the pathological changes, immune responses, and gut bacterial communities of pearl gentian grouper after exposure to differently virulent V. harveyi strains. Obvious histopathological changes were detected in heart, kidney, and liver. In particular, nodules appeared and huge numbers of V. harveyi cells colonized the liver at 12 h postinfection (hpi) with highly virulent V. harveyi. Although no V. harveyi was detected in the gut, the infection simultaneously induced a gut-liver immune response. In particular, the expression of 8 genes associated with cellular immune processes, including genes encoding inflammatory cytokines and receptors, and pattern recognition proteins, was markedly induced by V. harveyi infection, especially with the highly virulent V. harveyi strain. V. harveyi infection also induced significant changes in gut bacterial community, in which Vibrio and Photobacterium increased but Bradyrhizobium, Lactobacillus, Blautia, and Faecalibaculum decreased in the group infected with the highly virulent strain, with accounting for 82.01% dissimilarity. Correspondingly, four bacterial functions related to bacterial pathogenesis were increased by infection with highly virulent V. harveyi, whereas functions involving metabolism and genetic information processing were reduced. These findings indicate that V. harveyi colonizes the liver and induces a gut-liver immune response that substantially disrupts the composition of and interspecies interactions in the bacterial community in fish gut, thereby altering the gut-microbiota-mediated functions and inducing fish death.

Dataset Information

Multiomics analysis of soybean meal induced marine fish enteritis in juvenile pearl gentian grouper, Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂.

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