Rumen DNA virome and its relationship with feed efficiency in dairy cows.

IF 13.8 1区生物学 Q1 MICROBIOLOGY

Microbiome Pub Date : 2025-01-16 DOI:10.1186/s40168-024-02019-0

Xiaohan Liu, Yifan Tang, Hongyi Chen, Jian-Xin Liu, Hui-Zeng Sun

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引用次数: 0

Abstract

Background: The rumen harbors a diverse virome that interacts with other microorganisms, playing pivotal roles in modulating metabolic processes within the rumen environment. However, the characterization of rumen viruses remains incomplete, and their association with production traits, such as feed efficiency (FE), has not been documented. In this study, rumen fluid from 30 Chinese Holstein dairy cows was analyzed using next-generation sequencing (NGS) and High-Fidelity (HiFi) sequencing to elucidate the rumen DNA virome profile and uncover potential viral mechanisms influencing FE.

Results: Integrated NGS and HiFi sequencing enhanced the length, completeness, and resolution of viral operational taxonomic units (vOTUs) compared to NGS. A total of 6,922 vOTUs were identified, including 4,716 lytic and 1,961 temperate vOTUs. At the family level, lytic viruses were predominantly from Siphoviridae (30.35%) and Schitoviridae (23.93%), while temperate viruses were primarily Siphoviridae (67.21%). The study annotated 2,382 auxiliary metabolic genes (AMGs), comprising 1,752 lytic virus-associated AMGs across 51 functional categories and 589 temperate virus-associated AMGs across 29 categories. Additionally, 2,232 vOTU-host metagenome-assembled genome (hMAG) linkages were predicted, with Firmicutes_A (33.60%) and Bacteroidota (33.24%) being the most prevalent host phyla. Significant differences in viral populations were observed between high and low FE groups across multiple taxonomic levels (P < 0.05). Two pathways were proposed to explain how rumen viruses might modulate FE: (1) Lytic viruses could lyse beneficial host bacteria linked to favorable cattle phenotypes, such as vOTU1836 targeting Ruminococcaceae, resulting in diminished organic acid production and consequently lower FE; (2) AMG-mediated host metabolism modulation, exemplified by GT2 carried by vOTU0897, which may enhance Lachnospiraceae fermentation capacity, increasing organic acid production and thereby improving FE.

Conclusions: This study constructed a comprehensive rumen DNA virome profile for Holstein dairy cows, elucidating the structural and functional complexity of rumen viruses, the roles of AMGs, and vOTU-hMAG linkages. The integration of these data offers novel insights into the mechanisms by which rumen viruses may regulate nutrient utilization, potentially influencing FE in dairy cows. Video Abstract.

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奶牛瘤胃DNA病毒组及其与饲料效率的关系

背景：瘤胃中有多种病毒，它们与其他微生物相互作用，在调节瘤胃环境中的代谢过程中起着关键作用。然而，瘤胃病毒的特征仍然不完整，它们与生产性状（如饲料效率（FE））的关系尚未得到证实。本研究利用新一代测序（NGS）和高保真度（HiFi）测序技术分析了30头中国荷斯坦奶牛的瘤胃液，以阐明瘤胃DNA病毒组谱，揭示影响瘤胃FE的潜在病毒机制。结果：与NGS相比，整合NGS和HiFi测序增强了病毒操作分类单位（vOTUs）的长度、完整性和分辨率。共鉴定出6,922个votu，其中裂解性votu 4,716个，温带votu 1,961个。在科水平上，裂解型病毒以Siphoviridae（30.35%）和Schitoviridae（23.93%）为主，温带型病毒以Siphoviridae（67.21%）为主。该研究注释了2382个辅助代谢基因（AMGs），其中包括51个功能类别的1752个裂解病毒相关AMGs和29个类别的589个温带病毒相关AMGs。此外，预测了2232个votu -宿主宏基因组组装基因组（hMAG）连接，其中厚壁菌门（33.60%）和拟杆菌门（33.24%）是最普遍的宿主门。结论：本研究构建了荷斯坦奶牛瘤胃DNA病毒组图谱，阐明了瘤胃病毒的结构和功能复杂性、AMGs的作用以及vOTU-hMAG连锁反应。这些数据的整合为瘤胃病毒调节营养利用的机制提供了新的见解，可能影响奶牛的FE。视频摘要。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

Microbiome MICROBIOLOGY-

CiteScore

21.90

自引率

2.60%

发文量

198

审稿时长

4 weeks

期刊介绍： Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.