Metabolomics and proteomics insights into hepatic responses of weaned piglets to dietary Spirulina inclusion and lysozyme supplementation.

IF 2.3 2区 农林科学 Q1 VETERINARY SCIENCES BMC Veterinary Research Pub Date : 2024-11-06 DOI:10.1186/s12917-024-04339-7
Cátia Falcão Martins, Manolis Matzapetakis, David M Ribeiro, Josipa Kuleš, Anita Horvatić, Nicholas Guillemin, Peter David Eckersall, João P B Freire, André M Almeida, José A M Prates
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Abstract

Background: Studying the effect of dietary Spirulina and lysozyme supplementation on the metabolome and proteome of liver tissue contributes to understanding potential hepatic adaptations of piglets to these novel diets. This study aimed to understand the influence of including 10% Spirulina on the metabolome and proteome of piglet liver tissue. Three groups of 10 post-weaned piglets, housed in pairs, were fed for 28 days with one of three experimental diets: a cereal and soybean meal-based diet (Control), a base diet with 10% Spirulina (SP), and an SP diet supplemented with 0.01% lysozyme (SP + L). At the end of the trial, animals were sacrificed and liver tissue was collected. Metabolomics analysis (n = 10) was performed using NMR data analysed with PCA and PLS-DA. Proteomics analysis (n = 5) was conducted using a filter aided sample preparation (FASP) protocol and Tandem Mass Tag (TMT)-based quantitative approach with an Orbitrap mass spectrometer.

Results: Growth performance showed an average daily gain reduction of 9.5% and a feed conversion ratio increase of 10.6% in groups fed Spirulina compared to the control group. Metabolomic analysis revealed no significant differences among the groups and identified 60 metabolites in the liver tissue. Proteomics analysis identified 2,560 proteins, with 132, 11, and 52 differentially expressed in the Control vs. SP, Control vs. SP + L and SP vs. SP + L comparisons, respectively. This study demonstrated that Spirulina enhances liver energy conversion efficiency, detoxification and cellular secretion. It improves hepatic metabolic efficiency through alterations in fatty acid oxidation (e.g., upregulation of enzymes like fatty acid synthase and increased acetyl-CoA levels), carbohydrate catabolism (e.g., increased glucose and glucose-6-phosphate), pyruvate metabolism (e.g., higher levels of pyruvate and phosphoenolpyruvate carboxykinase), and cellular defence mechanisms (e.g., upregulation of glutathione and metallothionein). Lysozyme supplementation mitigates some adverse effects of Spirulina, bringing physiological responses closer to control levels. This includes fewer differentially expressed proteins and improved dry matter, organic matter and energy digestibility. Lysozyme also enhances coenzyme availability, skeletal myofibril assembly, actin-mediated cell contraction, tissue regeneration and development through mesenchymal migration and nucleic acid synthesis pathways.

Conclusions: While Spirulina inclusion had some adverse effects on growth performance, it also enhanced hepatic metabolic efficiency by improving fatty acid oxidation, carbohydrate catabolism and cellular defence mechanisms. The addition of lysozyme further improved these benefits by reducing some of the negative impacts on growth and enhancing nutrient digestibility, tissue regeneration, and overall metabolic balance. Together, Spirulina and lysozyme demonstrate potential as functional dietary components, but further optimization is needed to fully realize their benefits without compromising growth performance.

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代谢组学和蛋白质组学对断奶仔猪对日粮中添加螺旋藻和溶菌酶的肝脏反应的深入研究。
背景:研究日粮中添加螺旋藻和溶菌酶对肝组织代谢组和蛋白质组的影响有助于了解仔猪肝脏对这些新型日粮的潜在适应性。本研究旨在了解添加 10% 螺旋藻对仔猪肝组织代谢组和蛋白质组的影响。三组 10 头断奶后的仔猪成对饲养,用三种试验日粮中的一种饲喂 28 天:以谷物和豆粕为基础的日粮(对照组)、添加 10% 螺旋藻的基础日粮(SP)和添加 0.01% 溶菌酶的 SP 日粮(SP + L)。试验结束后,动物被处死并收集肝脏组织。利用 PCA 和 PLS-DA 分析的 NMR 数据进行代谢组学分析(n = 10)。蛋白质组学分析(n = 5)采用过滤辅助样品制备(FASP)方案和基于串联质谱标签(TMT)的定量方法,使用 Orbitrap 质谱仪进行:生长性能显示,与对照组相比,饲喂螺旋藻组的平均日增重降低了 9.5%,饲料转化率提高了 10.6%。代谢组学分析表明,各组之间没有显著差异,肝脏组织中发现了 60 种代谢物。蛋白质组学分析确定了 2,560 种蛋白质,在对照组与 SP 组、对照组与 SP + L 组和 SP 组与 SP + L 组的比较中,分别有 132、11 和 52 种蛋白质表达不同。这项研究表明,螺旋藻能提高肝脏的能量转换效率、解毒能力和细胞分泌能力。螺旋藻通过改变脂肪酸氧化(如脂肪酸合成酶等酶的上调和乙酰-CoA水平的增加)、碳水化合物分解(如葡萄糖和葡萄糖-6-磷酸水平的增加)来提高肝脏代谢效率、丙酮酸代谢(如丙酮酸和磷酸烯醇丙酮酸羧激酶水平升高)和细胞防御机制(如谷胱甘肽和金属硫蛋白水平升高)。补充溶菌酶可减轻螺旋藻的一些不利影响,使生理反应更接近控制水平。这包括减少差异表达蛋白,提高干物质、有机物和能量的消化率。溶菌酶还能通过间质迁移和核酸合成途径,提高辅酶可用性、骨骼肌纤维组装、肌动蛋白介导的细胞收缩、组织再生和发育:虽然螺旋藻对生长性能有一些不利影响,但它也通过改善脂肪酸氧化、碳水化合物分解和细胞防御机制提高了肝脏代谢效率。溶菌酶的添加进一步改善了这些益处,减少了对生长的一些负面影响,提高了营养消化率、组织再生和整体代谢平衡。螺旋藻和溶菌酶共同展示了作为功能性膳食成分的潜力,但还需要进一步优化,才能在不影响生长性能的前提下充分发挥它们的优势。
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来源期刊
BMC Veterinary Research
BMC Veterinary Research VETERINARY SCIENCES-
CiteScore
4.80
自引率
3.80%
发文量
420
审稿时长
3-6 weeks
期刊介绍: BMC Veterinary Research is an open access, peer-reviewed journal that considers articles on all aspects of veterinary science and medicine, including the epidemiology, diagnosis, prevention and treatment of medical conditions of domestic, companion, farm and wild animals, as well as the biomedical processes that underlie their health.
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