Elevated levels of butyric acid in the jejunum of an animal model of broiler chickens: from early onset of Clostridium perfringens infection to clinical disease of necrotic enteritis

IF 7 1区 农林科学 Q1 Agricultural and Biological Sciences Journal of Animal Science and Biotechnology Pub Date : 2024-11-02 DOI:10.1186/s40104-024-01105-5
Hemlata Gautam, Noor Ahmad Shaik, Babajan Banaganapalli, Shelly Popowich, Iresha Subhasinghe, Lisanework E. Ayalew, Rupasri Mandal, David S. Wishart, Suresh Tikoo, Susantha Gomis
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Abstract

Necrotic enteritis (NE) is an economically important disease of broiler chickens caused by Clostridium perfringens (CP). The pathogenesis, or disease process, of NE is still not clear. This study aimed to identify the alterations of metabolites and metabolic pathways associated with subclinical or clinical NE in CP infected birds and to investigate the possible variations in the metabolic profile of birds infected with different isolates of CP. Using a well-established NE model, the protein content of feed was changed abruptly before exposing birds to CP isolates with different toxin genes combinations (cpa, cpb2, netB, tpeL; cpa, cpb2, netB; or cpa, cpb2). Metabolomics analysis of jejunal contents was performed by a targeted, fully quantitative LC-MS/MS based assay. This study detected statistically significant differential expression of 34 metabolites including organic acids, amino acids, fatty acids, and biogenic amines, including elevation of butyric acid at onset of NE in broiler chickens. Subsequent analysis of broilers infected with CP isolates with different toxin gene combinations confirmed an elevation of butyric acid consistently among 21 differentially expressed metabolites including organic acids, amino acids, and biogenic amines, underscoring its potential role during the development of NE. Furthermore, protein-metabolite network analysis revealed significant alterations in butyric acid and arginine-proline metabolisms. This study indicates a significant metabolic difference between CP-infected and non-infected broiler chickens. Among all the metabolites, butyric acid increased significantly in CP-infected birds compared to non-infected healthy broilers. Logistic regression analysis revealed a positive association between butyric acid (coefficient: 1.23, P < 0.01) and CP infection, while showing a negative association with amino acid metabolism. These findings suggest that butyric acid could be a crucial metabolite linked to the occurrence of NE in broiler chickens and may serve as an early indicator of the disease at the farm level. Further metabolomic experiments using different NE animal models and field studies are needed to determine the specificity and to validate metabolites associated with NE, regardless of predisposing factors.
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肉鸡动物模型空肠中丁酸水平的升高:从早期感染产气荚膜梭菌到坏死性肠炎的临床发病过程
坏死性肠炎(NE)是由产气荚膜梭菌(CP)引起的肉鸡的一种重要经济疾病。坏死性肠炎的发病机制或疾病过程尚不清楚。本研究旨在确定受 CP 感染的禽类体内与亚临床或临床 NE 相关的代谢物和代谢途径的变化,并调查受不同 CP 分离物感染的禽类在代谢方面可能存在的变化。利用一个成熟的NE模型,在鸟类接触具有不同毒素基因组合(cpa、cpb2、netB、tpeL;cpa、cpb2、netB;或cpa、cpb2)的CP分离物之前,突然改变饲料中的蛋白质含量。空肠内容物的代谢组学分析是通过一种基于靶向、完全定量的 LC-MS/MS 方法进行的。该研究检测到 34 种代谢物(包括有机酸、氨基酸、脂肪酸和生物胺)存在统计学意义上的差异表达,其中包括肉鸡 NE 发病时丁酸的升高。随后对感染了具有不同毒素基因组合的 CP 分离物的肉鸡进行的分析证实,在包括有机酸、氨基酸和生物胺在内的 21 种差异表达代谢物中,丁酸的表达量一直在升高,这突显了丁酸在 NE 发生过程中的潜在作用。此外,蛋白质代谢物网络分析显示,丁酸和精氨酸-脯氨酸代谢发生了显著变化。这项研究表明,感染氯化石蜡的肉鸡与未感染氯化石蜡的肉鸡在代谢方面存在明显差异。在所有代谢物中,与未感染 CP 的健康肉鸡相比,感染 CP 的肉鸡体内的丁酸明显增加。逻辑回归分析表明,丁酸(系数:1.23,P < 0.01)与CP感染呈正相关,而与氨基酸代谢呈负相关。这些研究结果表明,丁酸可能是与肉鸡NE发生相关的重要代谢物,可作为鸡场的早期疾病指标。需要利用不同的 NE 动物模型和现场研究开展进一步的代谢组学实验,以确定特异性并验证与 NE 相关的代谢物,而不考虑易感因素。
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来源期刊
Journal of Animal Science and Biotechnology
Journal of Animal Science and Biotechnology AGRICULTURE, DAIRY & ANIMAL SCIENCE-
CiteScore
9.90
自引率
2.90%
发文量
822
审稿时长
17 weeks
期刊介绍: Journal of Animal Science and Biotechnology is an open access, peer-reviewed journal that encompasses all aspects of animal science and biotechnology. That includes domestic animal production, animal genetics and breeding, animal reproduction and physiology, animal nutrition and biochemistry, feed processing technology and bioevaluation, animal biotechnology, and meat science.
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