{"title":"Caecal metabolomics of two divergently selected rabbit lines revealed microbial mechanisms correlated to intramuscular fat deposition.","authors":"Agostina Zubiri-Gaitán, Marina Martínez-Álvaro, Agustín Blasco, Pilar Hernández","doi":"10.1093/jas/skae339","DOIUrl":null,"url":null,"abstract":"<p><p>The gastrointestinal microbiota plays a key role in the host physiology and health through a complex host-microbiota co-metabolism. Metabolites produced by microbial metabolism can travel through the bloodstream to reach distal organs and affect their function, ultimately influencing the development of relevant production traits such as meat quality. Meat quality is a complex trait made up of a number of characteristics and intramuscular fat content (IMF) is considered to be one of the most important parameters. In this study, 52 rabbits from two lines divergently selected for IMF (high-IMF (H) and low-IMF (L) lines) were used to perform an untargeted metabolomic analysis of their caecal content, with the aim to obtain information on genetically determined microbial metabolism related to IMF. A large, correlated response to selection was found in their caecal metabolome composition. Partial least squares discriminant analysis was used to identify the pathways differentiating the lines, which showed a classification accuracy of 99%. On the other hand, two linear partial least squares analyses were performed, one for each line, to extract evidence on the specific pathways associated with IMF deposition within each line, which showed predictive abilities (estimated using the Q2) of approximately 60%. The most relevant pathways differentiating the lines were those related to amino acids (aromatic, branched-chain and gamma-glutamyl), secondary bile acids, and purines. The higher content of secondary bile acids in the L-line was related to greater lipid absorption, while the differences found in purines suggested different fermentation activities, which could be related to greater nitrogen utilisation and energy efficiency in the L-line. The linear analyses showed that lipid metabolism had a greater relative importance for IMF deposition in the L-line, whereas a more complex microbial metabolism was associated in the H-line. The lysophospholipids and gamma-glutamyl amino acids were associated with IMF in both lines; the nucleotide and secondary bile acid metabolisms were mostly associated in the H-line; and the long-chain and branched-chain fatty acids were mostly associated in the L-line. A metabolic signature consisting of two secondary bile acids and two protein metabolites was found with 88% classification accuracy, pointing to the interaction between lipid absorption and protein metabolism as a relevant driver of the microbiome activity influencing IMF.</p>","PeriodicalId":14895,"journal":{"name":"Journal of animal science","volume":null,"pages":null},"PeriodicalIF":2.7000,"publicationDate":"2024-11-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of animal science","FirstCategoryId":"97","ListUrlMain":"https://doi.org/10.1093/jas/skae339","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"AGRICULTURE, DAIRY & ANIMAL SCIENCE","Score":null,"Total":0}
引用次数: 0
Abstract
The gastrointestinal microbiota plays a key role in the host physiology and health through a complex host-microbiota co-metabolism. Metabolites produced by microbial metabolism can travel through the bloodstream to reach distal organs and affect their function, ultimately influencing the development of relevant production traits such as meat quality. Meat quality is a complex trait made up of a number of characteristics and intramuscular fat content (IMF) is considered to be one of the most important parameters. In this study, 52 rabbits from two lines divergently selected for IMF (high-IMF (H) and low-IMF (L) lines) were used to perform an untargeted metabolomic analysis of their caecal content, with the aim to obtain information on genetically determined microbial metabolism related to IMF. A large, correlated response to selection was found in their caecal metabolome composition. Partial least squares discriminant analysis was used to identify the pathways differentiating the lines, which showed a classification accuracy of 99%. On the other hand, two linear partial least squares analyses were performed, one for each line, to extract evidence on the specific pathways associated with IMF deposition within each line, which showed predictive abilities (estimated using the Q2) of approximately 60%. The most relevant pathways differentiating the lines were those related to amino acids (aromatic, branched-chain and gamma-glutamyl), secondary bile acids, and purines. The higher content of secondary bile acids in the L-line was related to greater lipid absorption, while the differences found in purines suggested different fermentation activities, which could be related to greater nitrogen utilisation and energy efficiency in the L-line. The linear analyses showed that lipid metabolism had a greater relative importance for IMF deposition in the L-line, whereas a more complex microbial metabolism was associated in the H-line. The lysophospholipids and gamma-glutamyl amino acids were associated with IMF in both lines; the nucleotide and secondary bile acid metabolisms were mostly associated in the H-line; and the long-chain and branched-chain fatty acids were mostly associated in the L-line. A metabolic signature consisting of two secondary bile acids and two protein metabolites was found with 88% classification accuracy, pointing to the interaction between lipid absorption and protein metabolism as a relevant driver of the microbiome activity influencing IMF.
胃肠道微生物群通过复杂的宿主-微生物群协同代谢对宿主的生理和健康起着关键作用。微生物代谢产生的代谢物可通过血液到达远端器官并影响其功能,最终影响肉质等相关生产性状的发展。肉质是由多种特征组成的复杂性状,而肌肉内脂肪含量(IMF)被认为是最重要的参数之一。在这项研究中,研究人员利用从两个因肌内脂肪含量而不同的品系(高肌内脂肪含量品系(H)和低肌内脂肪含量品系(L))中挑选出来的 52 只兔子,对它们的盲肠内容物进行了非靶向代谢组学分析,目的是获得与肌内脂肪含量有关的由基因决定的微生物代谢信息。在它们的盲肠代谢组组成中发现了大量与选择相关的反应。利用偏最小二乘判别分析确定了区分品系的途径,分类准确率达到 99%。另一方面,对每个品系进行了两次线性偏最小二乘法分析,以提取每个品系中与 IMF 沉积相关的特定途径的证据,结果显示预测能力(使用 Q2 估算)约为 60%。与氨基酸(芳香族氨基酸、支链氨基酸和γ-谷氨酰氨基酸)、仲胆汁酸和嘌呤有关的途径是区分各品系的最相关途径。L 系次生胆汁酸含量较高,这与脂质吸收能力较强有关,而嘌呤含量的差异表明发酵活动不同,这可能与 L 系氮利用率和能量效率较高有关。线性分析表明,脂质代谢对 L 线的 IMF 沉积具有更大的相对重要性,而 H 线的微生物代谢则更为复杂。溶血磷脂和γ-谷氨酰氨基酸在两个品系中都与IMF有关;核苷酸和次级胆汁酸代谢主要与H品系有关;长链脂肪酸和支链脂肪酸主要与L品系有关。由两种次级胆汁酸和两种蛋白质代谢物组成的代谢特征的分类准确率为 88%,表明脂质吸收和蛋白质代谢之间的相互作用是影响 IMF 的微生物组活动的相关驱动因素。
期刊介绍:
The Journal of Animal Science (JAS) is the premier journal for animal science and serves as the leading source of new knowledge and perspective in this area. JAS publishes more than 500 fully reviewed research articles, invited reviews, technical notes, and letters to the editor each year.
Articles published in JAS encompass a broad range of research topics in animal production and fundamental aspects of genetics, nutrition, physiology, and preparation and utilization of animal products. Articles typically report research with beef cattle, companion animals, goats, horses, pigs, and sheep; however, studies involving other farm animals, aquatic and wildlife species, and laboratory animal species that address fundamental questions related to livestock and companion animal biology will be considered for publication.