Convergent Evolution of Rumen Microbiomes in High-Altitude Mammals

• Published in: Current biology Vol. 26; no. 14; pp. 1873 - 1879
• Main Authors: Zhang, Zhigang, Xu, Dongming, Wang, Li, Hao, Junjun, Wang, Jinfeng, Zhou, Xin, Wang, Weiwei, Qiu, Qiang, Huang, Xiaodan, Zhou, Jianwei, Long, Ruijun, Zhao, Fangqing, Shi, Peng
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 25.07.2016
• Subjects: Adaptation, Physiological; Altitude; Animals; Biological Evolution; Cattle - microbiology; China; Gastrointestinal Microbiome - genetics; High-Throughput Nucleotide Sequencing; Metagenome; Sheep, Domestic - microbiology
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2016.05.012

Studies of genetic adaptation, a central focus of evolutionary biology, most often focus on the host’s genome and only rarely on its co-evolved microbiome. The Qinghai-Tibetan Plateau (QTP) offers one of the most extreme environments for the survival of human and other mammalian species. Yaks (Bos grunniens) and Tibetan sheep (T-sheep) (Ovis aries) have adaptations for living in this harsh high-altitude environment, where nomadic Tibetan people keep them primarily for food and livelihood [1]. Adaptive evolution affects energy-metabolism-related genes in a way that helps these ruminants live at high altitude [2, 3]. Herein, we report convergent evolution of rumen microbiomes for energy harvesting persistence in two typical high-altitude ruminants, yaks and T-sheep. Both ruminants yield significantly lower levels of methane and higher yields of volatile fatty acids (VFAs) than their low-altitude relatives, cattle (Bos taurus) and ordinary sheep (Ovis aries). Ultra-deep metagenomic sequencing reveals significant enrichment in VFA-yielding pathways of rumen microbial genes in high-altitude ruminants, whereas methanogenesis pathways show enrichment in the cattle metagenome. Analyses of RNA transcriptomes reveal significant upregulation in 36 genes associated with VFA transport and absorption in the ruminal epithelium of high-altitude ruminants. Our study provides novel insights into the contributions of microbiomes to adaptive evolution in mammals and sheds light on the biological control of greenhouse gas emissions from livestock enteric fermentation. [Display omitted] •High-altitude adaptation produces convergent phenotypes of rumen metabolism•Microbial community structures and compositions contribute to convergent adaptation•Results show convergence of microbial genes in VFAs and methane-yielding pathways•Microbiomes co-evolve with host genomes for extremely environmental adaptation Zhang et al. observe both low-methane emissions and high-VFA production in high-altitude mammals. Using ultra-deep metagenomic sequencing, the authors show co-enrichment in VFA-yielding pathways of rumen microbial genes in high-altitude species, suggesting convergent evolution of rumen microbiomes for their hosts’ energy harvesting persistence.