Juan Deng1,2,7, Ya-Jing Liu1,7, Wen-Tian Wei1, Qi-Xuan Huang1, Li-Ping Zhao3,4, Ling-Yun Luo1, Qi Zhu2, Lin Zhang2, Yuan Chen2, Yan-Ling Ren5, Shan-Gang Jia6, Yu-Luan Lin1, Ji Yang1, Feng-Hua Lv1, Hong-Ping Zhang2, Feng-E Li4, Li Li2 and Meng-Hua Li1 1College of Animal Science and Technology, China Agricultural University, Beijing 100193, China; 2Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China; 3CAS Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences (CAS), Beijing 100101, China; 4Key Laboratory of Agricultural Animal Genetics, Breeding, and Reproduction of the Ministry of Education and Key Laboratory of Swine Genetics and Breeding of Ministry of Agriculture and Rural Affairs, Huazhong Agricultural University, Wuhan 430070, China; 5Shandong Binzhou Academy of Animal Science and Veterinary Medicine, Binzhou 256600, China; 6College of Grassland Science and Technology, China Agricultural University, Beijing 100193, China

↵7 These authors contributed equally to this work.

Corresponding authors: menghua.licau.edu.cn, lilysicau.edu.cn Abstract

The rumen undergoes developmental changes during maturation. To characterize this understudied dynamic process, we profiled single-cell transcriptomes of about 308,000 cells from the rumen tissues of sheep and goats at 17 time points. We built comprehensive transcriptome and metagenome atlases from early embryonic to rumination stages, and recapitulated histomorphometric and transcriptional features of the rumen, revealing key transitional signatures associated with the development of ruminal cells, microbiota, and core transcriptional regulatory networks. In addition, we identified and validated potential cross-talk between host cells and microbiomes and revealed their roles in modulating the spatiotemporal expression of key genes in ruminal cells. Cross-species analyses revealed convergent developmental patterns of cellular heterogeneity, gene expression, and cell–cell and microbiome–cell interactions. Finally, we uncovered how the interactions can act upon the symbiotic rumen system to modify the processes of fermentation, fiber digestion, and immune defense. These results significantly enhance understanding of the genetic basis of the unique roles of rumen.

Footnotes

[Supplemental material is available for this article.]

Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.278239.123.

Freely available online through the Genome Research Open Access option.

Received June 30, 2023. Accepted September 17, 2023.