从油茶籽提取的茶皂素对猪源多重耐药产肠毒素大肠杆菌的体外抑菌效果

doi:10.11843/j.issn.0366-6964.2025.05.041

摘要/Abstract

摘要：

本研究旨在探索茶皂素对猪源多重耐药性产肠毒素大肠杆菌(enterotoxigenic E.coli, ETEC)的抑菌效果，并解析其抑菌机制，为防控ETEC感染引起的仔猪腹泻提供新思路。本研究首先采用标准的纸片扩散法，评估所选取的猪源ETEC菌株对一系列抗生素的敏感性，并利用96孔微量肉汤稀释法测定抗生素及茶皂素对该ETEC菌株的最小抑菌浓度(MIC)。通过对比有无茶皂素处理条件下，该ETEC菌株的生长曲线变化、超微结构变化，以及胞内核酸、蛋白质和碱性磷酸酶等物质的泄漏情况，明确茶皂素对猪源多重耐药性ETEC的抑菌作用。此外，还采用转录组学技术分析有无茶皂素处理条件下细菌基因表达谱的差异，揭示茶皂素对该猪源ETEC的抑菌作用机制。此外，利用CCK-8方法评估茶皂素在猪小肠上皮细胞(IPEC-J2)上的安全性和有效性。药敏试验结果显示，该猪源ETEC菌株对临床常用的14种抗生素中的9种具有耐药性，属于多重耐药菌株。而茶皂素的MIC为50 mg·mL^-1，在1×MIC和2×MIC的浓度下，它对猪源多重耐药ETEC菌株展现出较强的抑菌活性，能在12 h的作用时间内有效抑制该ETEC菌株的生长和繁殖。经过1×MIC和2×MIC浓度的茶皂素处理后，细菌的形态结构发生显著变化。具体表现为细菌细胞结构受到严重破坏，导致细菌胞外的核酸、可溶性蛋白质以及碱性磷酸酶的浓度在最初的2 h内显著性上升，并且在整个12 h的观察期内，这些物质的浓度均显著高于对照组，最终导致细菌的死亡。SDS-PAGE电泳结果显示，经过茶皂素处理的ETEC菌株，在相对分子质量15~25 ku的蛋白质条带明显减少。转录组分析进一步揭示，茶皂素的抑菌机制可能涉及多个层面，包括抑制脂多糖的生物合成、影响核糖体的功能以及干扰细菌蛋白质的合成过程等相关通路。此外，研究还发现，在0.781~12.5 μg·mL^-1的浓度，茶皂素对IPEC-J2细胞无明显的毒副作用。特别地，在12.5 μg·mL^-1的浓度下，茶皂素能显著提高IPEC-J2细胞在受到ETEC感染后的存活率。综上所述，茶皂素对猪源多重耐药性ETEC菌株具有显著的抑菌活性，其抑菌机制复杂且多层面。研究结果为茶皂素作为天然抑菌剂在畜牧业中的应用提供了理论支持。

关键词: 茶皂素, 多重耐药, 猪源产肠毒素大肠杆菌, 抑菌活性, 抑菌机制

Abstract:

The study aimed to investigate the bacteriostatic activity and the underlying bacteriostatic mechanism of tea saponins against a strain of porcine-originated multidrug-resistant enterotoxigenic Escherichia coli (ETEC), ultimately providing novel perspectives for the prevention and control of piglet diarrhea caused by ETEC infection. The Kirby-Bauer disk diffusion method was utilized to assess a series of antibiotics sensitivity of the porcine-originated ETEC strain. Furthermore, the minimum inhibitory concentration (MIC) of antibiotics and tea saponins against the ETEC strain was determined through the 96-well plate broth microdilution method. To elucidate the bacteriostatic effect of tea saponins against the ETEC strain, a comparative analysis was conducted on the growth curve, ultrastructure, nucleic acid and protein leakage, alkaline phosphatase (AKP) activity between the tea saponins treated and untreated samples. Meanwhile, transcriptomic technology was utilized to analyze the differences in bacterial gene expression profiles under the conditions of tea saponins treatment and non-tea saponins treatment, revealing the bacteriostatic mechanism of tea saponins on this porcine ETEC. Additionally, the safety and efficacy of tea saponins on IPEC-J2 cells were assessed utilizing the Cell Counting kit-8 assay. The drug sensitivity results indicated that the porcine-originated ETEC strain exhibited resistance to 9 out of the 14 commonly used antibiotics in clinical practice, classifying it as a multidrug-resistant strains. The MIC of tea saponins was 50 mg·mL^-1. At the tea saponins concentrations of 1×MIC and 2×MIC, it exhibited strong bacteriostatic activity against the porcine-originated multidrug-resistant ETEC strain, effectively inhibiting the growth and reproduction of the ETEC strain within 12 h. After treatment with tea saponins at 1×MIC and 2×MIC concentrations, the bacteria morphological structure was significant damaged, resulting in a significant increase in the concentration of nucleic acid, soluble protein, and AKP in the extracellular bacterial cells within the initial 2 h. Moreover, during the entire 12 h observation period, the concentrations of these substances were significantly higher than those in the control group, ultimately triggering to the death of bacteria. SDS-PAGE electrophoresis result revealed that the protein bands within the molecular weight range of 15-25 ku in the ETEC strain treated with tea saponins were significantly reduced. Transcriptome analysis further indicated that the bacteriostatic mechanisms of tea saponins might involve multiple levels, including the suppression of lipopolysaccharide biosynthesis, ribosomal function, protein synthesis processes and other related pathways. In addition, the study discovered that within the concentration range of 0.781-12.5 μg·mL^-1, tea saponins exhibited no discernible toxic side effects on IPEC-J2 cells. Particularly, at a concentration of 12.5 μg·mL^-1, tea saponins significantly enhanced the survival rate of IPEC-J2 cells after ETEC infection. In conclusion, tea saponins exhibited significant bacteriostatic effects against porcine-originated multidrug-resistant ETEC strain, with its bacteriostatic mechanisms being intricated and multifaceted. The results provide theoretical support for the application of tea saponins as a natural bacteriostatic agent in animal husbandry.

Key words: tea saponins, multidrug resistant, porcine-originated enterotoxigenic Escherichia coli, bacteriostatic activity, bacteriostatic mechanism

中图分类号:

S853.7

梁莉雯, 李军星, 袁秀芳, 余斌, 叶十一, 徐丽华, 苏菲, 刘璨颖. 从油茶籽提取的茶皂素对猪源多重耐药产肠毒素大肠杆菌的体外抑菌效果[J]. 畜牧兽医学报, 2025, 56(5): 2451-2465.

LIANG Liwen, LI Junxing, YUAN Xiufang, YU Bin, YE Shiyi, XU Lihua, SU Fei, LIU Canying. In vitro Evaluation of the Bacteriostatic Efficacy of Tea Saponins Derived from Camellia oleifera Seeds against a Multidrug-resistant Enterotoxigenic Escherichia coli Strain Isolated from Pigs[J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(5): 2451-2465.

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抗生素名称 Antibiotic name	判定标准(抑菌圈直径/mm) Determination riterion(inhibition zones, mm)			抑菌圈直径/mm Inhibitory zone diameter	药物敏感性 Drug susceptibility
抗生素名称 Antibiotic name	S	I	R	抑菌圈直径/mm Inhibitory zone diameter	药物敏感性 Drug susceptibility
头孢噻肟Cefotaxime	≥26	23~25	≤22	17	R
头孢噻吩Cefalotin	≥18	15-17	≤14	12	R
阿莫西林Amoxicillin	≥17	14~16	≤13	16	I
氨苄西林Ampicillin	≥17	14~16	≤13	17	S
青霉素Penicillin	≥17	14~16	≤13	8	R
庆大霉素Gentamicin	≥15	13~14	≤12	22	S
卡那霉素Kanamycin	≥18	14~17	≤13	6	R
阿米卡星Amikacin	≥17	15~16	≤14	18	S
链霉素Streptomycin	≥15	12~14	≤11	11	R
多西环素Doxycycline	≥14	11~13	≤10	12	I
红霉素Erythromycin	≥17	11~15	≤10	10	R
四环素Tetracycline	≥15	12~14	≤11	8	R
甲氧苄啶-磺胺甲噁唑 Sulfamethoxazole-Trimethoprim	≥16	11~15	≤10	6	R
环丙沙星Ciprofloxacin	≥26	22~25	≤21	16	R

抗生素名称 Antibiotic name	判定标准[MIC/(μg·mL^-1)] Determination riterion(MIC, μg·mL^-1)			MIC/(μg·mL^-1)	药物敏感性 Drug susceptibility
抗生素名称 Antibiotic name	S	I	R	MIC/(μg·mL^-1)	药物敏感性 Drug susceptibility
氨苄西林Ampicillin	≤8	16	≥32	2	S
庆大霉素Gentamicin	≤4	8	≥16	0.5	S
四环素Tetracycline	≤4	8	≥16	32	R
甲氧氨苄-磺胺甲噁唑 Sulfamethoxazole-Trimethoprim	≤2/38	-	≥4/76	＞32/608	R

茶皂素浓度 Tea saponins concentrations	抑菌圈直径 Inhibitory zone diameter
2×MIC	9
1×MIC	8
1/2×MIC	6

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