Bacterial communities related to 3-nitro-1-propionic acid degradation in the rumen of grazing ruminants in the Qinghai-Tibetan Plateau

Authors: GUO, WEI - Lanzhou University; BI, SISI - Lanzhou University; KANG, JINGPENG - Lanzhou University; ZHANG, YING - Lanzhou University; LONG, RUIJUN - Lanzhou University; HUANG, XIAODAN - Lanzhou University; SHAN, M - Lanzhou University; Anderson, Robin

Submitted to: Anaerobe
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/31/2018
Publication Date: 12/1/2018
Citation: Guo, W., Bi, S., Kang, J., Zhang, Y., Long, R., Huang, X., Shan, M.N., Anderson, R.C. 2018. Bacterial communities related to 3-nitro-1-propionic acid degradation in the rumen of grazing ruminants in the Qinghai-Tibetan Plateau. Anaerobe. 54:42-54. https://doi.org/10.1016/j.anaerobe.2018.07.013.
DOI: https://doi.org/10.1016/j.anaerobe.2018.07.013

Interpretive Summary: The Qinghai-Tibetan Plateau of China is a unique high elevation habitat that supports a number of different toxic plants that are native to this environment. Farmers in this region raise yak and sheep and have reported that breeds that have lived in this habitat for thousands of years are more resistant to being poisoned by the toxic plants than sheep breeds recently introduced from the lowlands. To investigate if the native yak and sheep breeds may harbor microbes within their gastrointestinal tracts that are able to degrade some of these poisons, we collected gastrointestinal samples from 3 native yak, 3 native sheep, and 3 sheep of an introduced breed. When these gastrointestinal samples were cultured with a poisonous compound common to this region, nitropropionate, we observed no difference in ability of the microbial populations in those samples to degrade the poison. When we used molecular tests to characterize the microbial populations in the gastrointestinal samples, we found that the microbial population in the yak appeared specialized in its ability to metabolize high energy compounds such as fatty acids, whereas the microbial population in the sheep native to the Qinghai-Tibetan Plateau appeared to be specialized in metabolizing compounds such as proteins. Conversely, the microbial populations in the sheep that originated from the lowlands appeared to be specialized in producing methane as a non-usable end product, which might explain why these sheep may be less efficient at metabolizing grasses on the Qinghai-Tibetan Plateau than the animals native to this region. These results help explain why some animals perform better in different pasture regions than others. This may ultimately help farmers and ranchers in the U.S. and around the world learn how to better raise their animals as to more efficiently provide safe and wholesome food and milk at a lower cost.

Technical Abstract: The objectives of this study were to characterize the overall rumen bacterial community from grazing yak and sheep reared in the unique environmental conditions of the Qinghai-Tibetan Plateau as well as the microbial community associated with detoxification of the phytotoxin, 3-nitro-1-propionic acid (NPA), during in vitro culture with 4.2 mM NPA. Using 16S rRNA gene high-throughput sequencing we found that the yak rumen harbored populations with a higher alpha diversity than that in Tibetan sheep and the rumen bacterial community in the three ruminant species clearly differs from one another. PICRUSt analysis identified that the pathway involved in nitrogen metabolism was enriched in Tibetan sheep while that related to fatty acid biosynthesis was over-represented in yak. The methane metabolism pathway was predominant in small-tailed sheep. Comparisons between freshly collected rumen fluid and populations subjected to consecutive 72 h batch cultures revealed substantial decreases in alpha diversity in populations cultured with NPA. Moreover, the relative abundances of some bacterial taxa changed significantly, with Proteobacteria and Actinobacteria being increased in abundance. Additionally, the overall bacterial community between rumen fluid and cultures were clearly separated. With regard to PICRUSt analysis, the methane metabolism pathway became scarce in Tibetan sheep and small-tailed sheep, whereas the energy and carbohydrate metabolic pathways such as nitrogen metabolism, ABC transporters, and glycolysis/gluconeogenesis were significantly plentiful across groups.