Protective role of oligochitosan in intestinal homeostasis to Edwardsiella ictaluri in hybrid grouper (Epinephelus fuscoguttatus ♀ × Epinephelus lanceolatus ♂)

IF 3.9 1区农林科学 Q1 FISHERIES

Aquaculture Pub Date : 2025-07-02 DOI:10.1016/j.aquaculture.2025.742923

Lixin Ma, Zhilong Chen, Zhuojin He, Xiaomin Zheng, Yutao Li, Cuiyun Zhou, Li Lin, Fei Shi

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Abstract

Background

Edwardsiella ictaluri is a major pathogen that causes severe infections in fish. Oligochitosan has antioxidant and antibacterial properties, and can also regulate the immune system and intestinal flora.

Aims

In this study, we investigated the mechanisms of E. ictaluri infection in hybrid grouper and evaluated the effects of oligochitosan supplementation on intestinal health, gut microbiota, and metabolism.

Methods

In this study, we employed a combination of histopathology, TdT-mediated dUTP nick end labeling (TUNEL), biochemical analysis, 16S rRNA sequencing, fluorescence in situ hybridization (FISH), transcriptomics, and metabolomics.

Results

E. ictaluri infection significantly altered goblet cell counts (P < 0.05), apoptosis rates (P < 0.01), increased villus height (P < 0.05), and reduced muscularis thickness (P < 0.01). Oligochitosan intervention effectively restored intestinal structure. Compared to controls, E. ictaluri elevated intestinal superoxide dismutase (SOD) (P < 0.05) and amylase (AMS) activities (P < 0.01), while oligochitosan significantly decreased catalase (CAT) activity relative to infected fish (P < 0.01). The infection also increased bacterial load and disrupted microbiota composition, whereas oligochitosan promoted beneficial genera, including Faecalibaculum and Bacteroides. FISH analysis confirmed increased bacterial colonization post-infection (P < 0.01), which was alleviated by oligochitosan (P < 0.01). Transcriptomics revealed that E. ictaluri altered genes involved in fat absorption and TNF signaling, effects mitigated by oligochitosan. Metabolomics showed infection suppressed D-amino acid, taurine, and hypotaurine metabolism, reducing amino acid levels, while oligochitosan reversed these trends. Multi-omics correlation analyses indicated that oligochitosan modulated intestinal amino acid metabolism by enhancing probiotic-associated pathways.

Conclusion

Collectively, oligochitosan can alleviate E. ictaluri induced by enhancing intestinal tissue integrity and antioxidant defense, maintaining intestinal flora balance, and regulating amino acid metabolism.

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低聚壳聚糖在杂交石斑鱼（斑石斑鱼♀× lanceolatus Epinephelus♀）肠道内稳态中的保护作用

背景：伊塔卢氏矮人杆菌是引起鱼类严重感染的主要病原体。低聚壳聚糖具有抗氧化和抗菌的特性，还可以调节免疫系统和肠道菌群。目的在本研究中，我们研究了杂交石斑鱼伊克塔卢菌感染的机制，并评估了添加低聚壳聚糖对肠道健康、肠道微生物群和代谢的影响。方法采用组织病理学、tdt介导的dUTP nick end标记（TUNEL）、生化分析、16S rRNA测序、荧光原位杂交（FISH）、转录组学和代谢组学等方法对其进行检测。ictaluri感染显著改变杯状细胞计数(P <；0.05)，细胞凋亡率(P <；0.01)，绒毛高度增加(P <；0.05)，肌层厚度减少(P <；0.01)。低聚壳聚糖干预可有效恢复肠道结构。与对照组相比，伊卡卢杆菌升高了肠道超氧化物歧化酶（SOD） (P <；0.05)和淀粉酶（AMS）活性(P <；低壳聚糖显著降低过氧化氢酶（CAT）活性(P <；0.01)。感染还增加了细菌负荷并破坏了微生物群组成，而低壳聚糖促进了有益的属，包括Faecalibaculum和Bacteroides。FISH分析证实感染后细菌定植增加(P <；0.01)，低聚壳聚糖缓解了这一影响(P <；0.01)。转录组学显示，伊卡卢菌改变了参与脂肪吸收和TNF信号传导的基因，低聚壳聚糖减轻了这种影响。代谢组学显示，感染抑制了d -氨基酸、牛磺酸和次牛磺酸的代谢，降低了氨基酸水平，而低壳聚糖逆转了这些趋势。多组学相关分析表明，低聚壳聚糖通过增强益生菌相关途径调节肠道氨基酸代谢。结论低聚壳聚糖可通过增强肠道组织完整性和抗氧化防御、维持肠道菌群平衡、调节氨基酸代谢等途径减轻伊氏杆菌的诱导。

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来源期刊

Aquaculture 农林科学-海洋与淡水生物学

CiteScore

8.60

自引率

17.80%

发文量

1246

审稿时长

56 days

期刊介绍： Aquaculture is an international journal for the exploration, improvement and management of all freshwater and marine food resources. It publishes novel and innovative research of world-wide interest on farming of aquatic organisms, which includes finfish, mollusks, crustaceans and aquatic plants for human consumption. Research on ornamentals is not a focus of the Journal. Aquaculture only publishes papers with a clear relevance to improving aquaculture practices or a potential application.