Tang Yifan, Liu Xiaohan, Zhu Senlin, Jia Minghui, Liu Jian-Xin, Sun Hui-Zeng
Key Laboratory of Dairy Cow Genetic Improvement and Milk Quality Research of Zhejiang Province, College of Animal Sciences, Zhejiang University, Hangzhou 310058, PR China; Ministry of Education Key Laboratory of Molecular Animal Nutrition, Zhejiang University, Hangzhou 310058, PR China.
Key Laboratory of Dairy Cow Genetic Improvement and Milk Quality Research of Zhejiang Province, College of Animal Sciences, Zhejiang University, Hangzhou 310058, PR China; Ministry of Education Key Laboratory of Molecular Animal Nutrition, Zhejiang University, Hangzhou 310058, PR China; Ministry of Education Innovation Team of Development and Function of Animal Digestive System, Zhejiang University, Hangzhou 310058, PR China.
J Adv Res. 2024 Oct 18. doi: 10.1016/j.jare.2024.09.016.
As one of the important components of ruminant gastrointestinal tract (GIT) microbiome, archaea are involved in many biological processes, especially methanogenesis. In spite of being a well-recognised member of the mammalian gut microbiome, it remains poorly characterized, partly due to the lack of a unified reference genome catalog.
This study aimed to construct a unified genome atlas that captures the wider diversity in archaea and is thus more appropriate for functional and taxonomic exploration of ruminant GIT archaea.
We collected archaeal genomes from public sources and new data of this study. We performed phylogenetic and functional genomics analysis, prophage identification based on the genomes. Using collected genomes as a reference, we conducted metagenomic and metatranscriptomic analysis on rumen fluid samples from 18 dairy cows, and investigated the correlation between rumen archaeal communities and methane (CH) production profiles.
We constructed the ruminant GIT archaeal genomes (RGAG) by compiling 405 strain-level (160 species) non-redundant archaeal genomes from more than 10 ruminant species. Investigating the functional heterogeneity and methanogenic structure within RGAG revealed that it possessed 1,124 (99.5%) unknown microbial biosynthetic gene clusters. A survey of RGAG-borne prophages identified 63 prophages with 122 host-beneficial genes and 18 auxiliary metabolic genes. The pipeline for both metagenomics and metatranscriptomics generated in the study revealed the roles of archaeal genomes under-assessed in general multi-omics analysis. The highly expressed genus Methanosphaera was negatively correlated with CH production at the RNA level.
A unified genome atlas of ruminant GIT archaea is constructed in the study. Our analyses revealed the advantages of metatranscriptomics over metagenomics in studying rumen archaeal communities and further demonstrated that the multifaceted functions of ruminant archaea remain undiscovered. Differences in rumen archaeal community structure among cattle with different CH production profiles may reflect the balance between rumen hydrogen production and methanogenesis. Our work provides a new resource for interrogating archaeal functions in the ruminant GIT and potential targets for future CH reduction.
古菌作为反刍动物胃肠道（GIT）微生物群的重要组成部分，参与许多生物学过程，尤其是甲烷生成。尽管古菌是哺乳动物肠道微生物群中一个广为人知的成员，但其特征仍知之甚少，部分原因是缺乏统一的参考基因组目录。
本研究旨在构建一个统一的基因组图谱，以捕捉古菌更广泛的多样性，从而更适合对反刍动物GIT古菌进行功能和分类学探索。
我们从公共来源和本研究的新数据中收集古菌基因组。我们进行了系统发育和功能基因组学分析，基于基因组进行噬菌体鉴定。以收集到的基因组为参考，我们对18头奶牛的瘤胃液样本进行了宏基因组和宏转录组分析，并研究了瘤胃古菌群落与甲烷（CH）产生特征之间的相关性。
我们通过汇编来自10多种反刍动物的405个菌株水平（160个物种）的非冗余古菌基因组，构建了反刍动物GIT古菌基因组（RGAG）。对RGAG内的功能异质性和产甲烷结构进行研究发现，它拥有1124个（99.5%）未知的微生物生物合成基因簇。对RGAG携带的噬菌体进行调查，鉴定出63个噬菌体，其中有122个宿主有益基因和18个辅助代谢基因。本研究中生成的宏基因组和宏转录组分析流程揭示了在一般多组学分析中评估不足的古菌基因组的作用。在RNA水平上，高表达的甲烷球形菌属与CH产生呈负相关。
本研究构建了反刍动物GIT古菌的统一基因组图谱。我们的分析揭示了宏转录组学在研究瘤胃古菌群落方面相对于宏基因组学的优势，并进一步证明反刍动物古菌的多方面功能仍未被发现。不同CH产生特征的牛之间瘤胃古菌群落结构的差异可能反映了瘤胃产氢和甲烷生成之间的平衡。我们的工作为研究反刍动物GIT中古菌的功能提供了新资源，并为未来减少CH排放提供了潜在靶点。
